intensificación agrícola, biodiversidad y funcionamiento
TRANSCRIPT
Intensificación agrícola, biodiversidad y funcionamiento de la polinización
en la región Mediterránea
Agricultural intensification, biodiversity and pollination functioning in the Mediterranean region
Marian Mendoza Garcia
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Intensificación agrícola, biodiversidad y
funcionamiento de la polinización en la región Mediterránea
Agricultural intensification, biodiversity and pollination functioning in
the Mediterranean region
MARIAN MENDOZA GARCÍA
Barcelona, julio de 2018
Departamento de Biología Evolutiva,
Ecología y Ciencias Ambientales
Intensificación agrícola, biodiversidad y funcionamiento de la polinización en
la región Mediterránea
Agricultural intensification, biodiversity and pollination functioning in the Mediterranean region
Memoria presentada por Marian Mendoza García para optar por el grado de Doctora de la Universidad de Barcelona
Programa de Doctorado de Biodiversidad
Marian Mendoza García V°B° Director de Tesis V°B° Director de Tesis Dr. F. Xavier Sans Serra Dr. José M. Blanco Moreno
Barcelona, julio de 2018
Agradecimientos
A mis directores de tesis. A F. Xavier Sans, por su ejemplo de vida y trayectoria académica, su ayuda y apoyo, su estímulo y ánimo cuando el camino era arduo, y por la confianza depositada en mí durante toda la tesis. A José M. Blanco, por su incondicional apoyo y ayuda en cada paso, por su pedagógica guía, por enseñarme que la estadística estaba de mi parte, por mostrarme que en la ciencia todo tiene un valor, y sobre todo por creer en mí. To Péter Batáry, thank you very much for hosting me in your lab group and introducing me to the SEMs. I really appreciate your advice in those short-stays and your support in one of the manuscripts included in this thesis. I really enjoyed my time in Göttingen and I hope we will be able to work together in the future. To Rita, thanks for your kindness and friendship. It was great to share fieldwork with you, and I will always remember our wonderful coffee-time! To Francesco de Bello and Jan Lepš, thank you very much for accepting me in your team, for your time and the nice discussions. Thanks for your patience teaching me CANOCO and for your support in one of the manuscripts included in this thesis. I really enjoyed my time in České Budějovice (even in winter!). A Lourdes, por todo su apoyo y ayuda, especialmente en las largas jornadas de campo, por siempre tener una palabra amable y por su entrañable amistad. A Paola, por su amistad, su apoyo incondicional, su empatía y por los bonitos momentos compartidos. A Alex, por su ayuda y su paciencia, por sus conocimientos y por las horas infinitas bajo la lupa y entre moscas… Y también, por sus mandarinas. A David, Agnès, Roser, Laura A, Laura JM, Berta, Laura R, y a todos los que estuvieron de paso por el grupo, por las horas compartidas, por la ayuda y el apoyo, y por el ánimo… A Albert Ferré, por su inagotable paciencia y toda su ayuda cuando los mapas, especialmente los de mi tesis, perdían el norte y, a veces, hasta las capas.
A todas las personas del COFFEA, los constantes Arnau, Aaron, Pep, Empar, Esteve, Berta, Nuria, Estela, Alba, Marc, Eulàlia… y los no tan constantes, con los que aprendí datos sorprendentes, estadísticas mundiales, palabras curiosas y, lo mejor, por la compañía. A todas las personas del departamento, técnicos y personal administrativo, por la ayuda y colaboración brindada durante mi tesis. Al “Servei de Camps Experimentals”, especialmente a Josep Matas, por cuidar de mis plantas todas las primaveras. Al “Museu de Ciències Naturals de Barcelona”, por abrirme sus puertas y permitirme usar sus instalaciones. A Jorge Mederos, por su paciencia y su conocimiento, por las horas entre moscas y etiquetas… A Amador Viñolas, por su ayuda en la identificación de insectos. A Carla, Maru y Amanda, por los años juntas en distintas ciudades, en diferentes momentos, y espero que sean muchísimos más. A Laura, por todos los momentos juntas, por mostrarme Barcelona. A mi familia, mi mamá y mis hermanos, por su paciencia y comprensión, por saber escuchar, por su ayuda incondicional, por su cariño, y porque la distancia no es más que una palabra. Por los que hoy ya no están, pero perdura su recuerdo. A la familia Valencia-Gómez, por abrirme las puertas de su hogar y convertirse en mi familia. A Ariel, por su compañía y sus travesuras. A ti, Enrique, por tu paciencia, tu cariño, tu entrega y tu apoyo. Por mostrarme el camino, cuando parecía perdido. Por ser un pilar, cuando más lo necesité. Porque contigo, la vida se completa. Porque “esta tesis es tan tuya como mía”…
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RESUMEN
Síntesis……………………………………………………….…... 3
Summary (English version)..…….……………………….……… 6
Introducción……………………...…….………………………… 9
Intensificación agrícola, biodiversidad y servicios ecosistémicos…. 9 Los esquemas agroambientales como instrumento para la restauración del paisaje……………………………………….… 12 La comunidad vegetal, sus atributos funcionales y los visitantes florales en los sistemas agrícolas……………………................... 16 La polinización como servicio ecosistémico…………………… 19
Objetivos.………………………..………………………….……. 21
Metodología general……………………………………….…….. 24
Área de estudio………………………………………………… 24 Recursos florales…………………………………..………….. 27 Visitantes florales………………………………………………. 27 Especies diana y producción de frutos…………………..………. 29
CAPÍTULO 1: Agricultural landscape structure and field management have contrasting effects on the community of flower visiting insects and on the fruit set of target plants
Summary…..………………….…………………………….. 35
Introduction……………….………………….……………... 37
Material and methods….……………………….…….……... 42
Results……….…………………………….………………... 49
Discussion….………………………….……………………. 57
Conclusions.……...………….…….………………….…….. 65
References.…………………………….…………………..... 66
Supplementary material.…………….……………………..... 74
ÍNDICE
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CAPÍTULO 2: Farming practices and flower resources determine plant reproduction in Mediterranean landscapes
Summary…..………………….……………………………. 81
Introduction……………….………………….……………. 82
Material and methods….……………………….………….. 86
Results……….…………………………….………………. 91
Discussion….………………………….…………………… 95
Conclusions and management implications..……………… 99
References.…………………………….…………………... 100
Supplementary material.…………….……………………... 106
CAPÍTULO 3: Agricultural intensification at field and landscape levels affects flower visitors’ communities through changes in plant communities and their flower traits
Summary…..………………….……………………………. 113
Introduction……………….………………….……………. 115
Material and methods….……………………….………….. 119
Results……….…………………………….……………..... 125
Discussion….………………………….…………………… 130
Conclusions and management implications..……………… 134
References.…………………………….…………………... 135
Supplementary material.…………….……………………... 140
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CAPÍTULO 4: Patterns of flower visitor abundance and fruit set in a highly intensified cereal cropping system in a Mediterranean landscape
Summary…..………………….……………………………. 147
Introduction……………….………………….……………. 148
Material and methods….……………………….………….. 152
Results……….…………………………….………………. 159
Discussion….………………………….…………………… 164
Implications for management.……...………….…….…..… 168
References.…………………………….…………………... 169
Supplementary material.…………….……………………... 175
Discusión general………………………………………………….. 179
Conclusiones……………………………………………………..... 191
Implicaciones para la gestión y el desarrollo de medidas
agroambientales…………………………………………………. 194
Conclusions………………………………………………….…….. 196
Management implications and development of agri-environmental
measures………………………………………………………… 199
Referencias………………………………………………….……... 201
RESUMEN
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La intensificación agrícola es una de las principales causas de la pérdida de biodiversidad, así como de los servicios ecosistémicos asociados. Por una parte, la intensificación agrícola ha causado cambios en la estructura y en la composición del paisaje, mediante la reducción y simplificación de los hábitats naturales, lo que ha promovido la agregación de los campos y la baja heterogeneidad espacial. A nivel de parcela, la intensificación se genera por la aplicación reiterada y profusa de pesticidas y fertilizantes químicos, el laboreo intensivo y la simplificación en las rotaciones, produciendo una baja diversidad en la comunidad vegetal. Estos cambios en la estructura del paisaje y en la intensidad de la gestión se correlacionan con el declive de los polinizadores y, por ende, con los servicios de polinización que estos proveen, tanto a los cultivos como a las especies que habitan en los hábitats naturales y seminaturales no cultivados. La agricultura ecológica es una práctica agrícola respetuosa con el medio ambiente, considerada para mitigar el declive de los polinizadores y, en consecuencia, mejorar el servicio de la polinización. En comparación con la agricultura convencional, se ha demostrado que la agricultura ecológica tiene efectos positivos sobre la riqueza y la abundancia de las comunidades vegetales, lo que a su vez puede incrementar las visitas de los polinizadores. Además, algunos cultivos, como las leguminosas y los cultivos de floración masiva (colza), que son incluidos frecuentemente en las rotaciones de cultivos, también se benefician con el incremento de los visitantes florales. A su vez, estos cultivos también pueden influir en la actividad de los insectos, debido a que proveen abundantes recompensas de polen y néctar que pueden incrementar su abundancia. Todas estas complejas interacciones, finalmente, afectan la reproducción de las plantas. A pesar de ello, los efectos de la intensificación agrícola, el tipo de cultivo y la disponibilidad de los recursos florales sobre la abundancia y composición de los visitantes florales, así como sobre la producción de frutos de especies diana todavía no son comprendidos en su totalidad.
En la presente tesis, se evaluaron los efectos de la intensificación agrícola sobre la abundancia de los visitantes florales y la producción de frutos de especies diana (Capítulo 1). A nivel de paisaje, la intensificación agrícola afectó negativamente la abundancia de los visitantes florales, aunque este efecto dependió del grupo considerado. Asimismo, se evaluó la abundancia de los visitantes florales (apoideos) y la producción de frutos en paisajes que variaron en la proporción de tierra arable bajo gestión ecológica
SÍNTESIS
4
(Capítulo 2). A nivel de paisaje, la proporción de tierra arable bajo gestión ecológica no incrementó la abundancia de abejas (apoideos). A nivel de parcela, la agricultura ecológica tuvo un efecto positivo en la abundancia total de los visitantes florales, aunque las interacciones entre la gestión y el paisaje o la posición dentro del campo también dependieron del grupo de visitante floral. La abundancia de abejas tampoco incrementó en los márgenes aledaños a los cultivos de leguminosa, lo cual pudo ocurrir debido a una dilución de los visitantes florales causada por la abundante disponibilidad de recursos en el paisaje.
Nuestro estudio también analizó el efecto de la intensificación agrícola a nivel de paisaje y de parcela sobre la composición de la comunidad vegetal y de los visitantes florales, así como la relación entre la comunidad de visitantes florales y el “community-weighted mean” (CWM) de los atributos florales (Capítulo 3). La intensificación agrícola a nivel de paisaje se correlacionó con cambios en la composición florística de las comunidades vegetales de los márgenes de los campos y de algunos atributos florales de la comunidad (CWM). Por el contrario, en el centro de los campos la composición taxonómica de los ensamblajes de especies y el CWM de sus atributos florales respondieron, en gran medida, a las prácticas agrícolas a nivel de parcela. La composición de visitantes florales respondió a la intensificación agrícola a nivel de paisaje y a la composición vegetal en los márgenes de los campos. Además, nuestro estudio mostró que la respuesta de los visitantes florales a determinados atributos florales se mantuvo constante en ambos años de muestreo. Finalmente, los resultados señalaron que el color de la flor y la fenología de la comunidad vegetal afectaron la composición de los visitantes florales en el margen del campo, mientras que el tamaño de la flor influyó dicha composición en el centro del campo.
La intensificación agrícola a nivel de paisaje afectó negativamente la producción de frutos de la especie de polinización generalista. Sin embargo, el efecto del incremento de los recursos florales fue positivo sobre la producción de frutos (Capítulo 1). La proporción de tierra arable bajo gestión ecológica únicamente incrementó la proporción de frutos de la especie de polinización generalista, ya que no tuvo un efecto significativo sobre la especie de polinización especialista. La competencia por los visitantes florales pudo ocurrir entre las especies diana y las comunidades vegetales aledañas. A pesar de ello, los cultivos de leguminosa incrementaron la producción de frutos de ambas especies (Capítulo 2).
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Por último, se evaluó el efecto de la estructura del paisaje y la presencia de cultivos de floración masiva (cultivos de colza) sobre la abundancia de abejas (apoideos) y otros visitantes florales (coleópteros, dípteros y otros himenópteros), así como sobre la producción de frutos de dos especies diana (Capítulo 4). La presencia de cultivos de colza incrementó la abundancia de las abejas, aunque esta disminuyó en paisajes complejos (alta densidad de márgenes). Por otro lado, la abundancia de otros visitantes florales dependió de la estructura del paisaje, particularmente de la ubicación de los campos de cereales. A pesar del incremento en la abundancia y diversidad de los visitantes florales, promovida por los cultivos de colza y los recursos florales, solo incrementó la producción de frutos de la especie de polinización generalista, ya que la competencia por los visitantes florales pudo afectar a la especie de polinización especialista.
Nuestros resultados resaltan la importancia de la implementación de medidas agroambientales que contemplen, por una parte, evitar la simplificación del paisaje, así como promover la agricultura ecológica, incluir cultivos que ofrezcan recursos florales (cultivos de leguminosas y de floración masiva) y conservar los elementos de vegetación natural o seminatural, como son los márgenes de los campos. Dichas medidas permitirán optimizar el servicio de polinización, procurado por un amplio y diverso conjunto de visitantes florales en los paisajes agrícolas mediterráneos.
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Agricultural intensification is one of the main causes of biodiversity decline and disruption of associated ecosystem services. On the one hand, intensification at landscape scale has caused changes in the structure and composition of the landscape, through the substitution of most natural habitats with arable fields leading to large, uniformly-cropped areas, with low spatial heterogeneity. On the other hand, intensification at field scale occurs by use of a high amount of external inputs, intensive soil tillage and simplification of crop-rotational schemes, resulting in plant communities with low diversity within-fields and in neighbouring field margins. These changes in landscape structure and land-use intensity are generally correlated with the decline of wild pollinators and the services they provide to crops and wild plants. Organic farming practices are thought to mitigate pollinator decrease in agricultural landscapes and, in consequence, could improve pollination services. Compared with conventional farming, organically managed fields support higher levels of plant abundance and diversity, which in turn can attract more pollinator visits. Furthermore, some crops that are routinely included in crop rotations, such as legumes and some mass flowering crops as oilseed rape, also can benefit from the presence of flower visiting insects. In turn, these crops can influence the activity of the insects, as they constitute a highly rewarding resource of pollen and nectar that can enhance flower visitor abundance. These complex interactions can finally affect plant reproduction. Nevertheless, the effects of agricultural landscape at different levels, crop type and the availability of flower resources on the abundance and composition of flower visiting insects and the fruit set of insect-pollinated plants are not completely understood.
We evaluated the effects of agricultural land use intensity on the abundance of flower-visiting insects and on the fruit set of an insect pollinated target plant (Chapter 1). At landscape level, the percentage of arable land affected negatively the abundance of flower-visiting insects, although this effect was not consistent among the groups of flower visitors. Additionally, we evaluated the abundance of flower visitors (bees) and pollination delivery in landscapes varying in their proportion of organically managed arable land (Chapter 2). Bee abundance was not enhanced by the proportion of organically managed land at the landscape scale. At field level, we found that organic farming had a positive effect on the overall abundance of flower visitors, although the interactions between management and the
SUMMARY
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landscape or the position within the field also depended on the group of flower visitors. Bee abundance did not also increase in field margins next to legume crops, probably caused by abundant food resources that led to their dilution.
Our study also analysed compositional changes in plant and flower visitor communities in response to agricultural intensification at field and landscape levels, and the relation between the insect community and the community-weighted mean (CWM) of flower traits (Chapter 3). On the one hand, plant species composition and the CWM in field centre responded to field management, whereas in the margin depended on the percentage of arable land. On the other hand, flower visitor composition only responded to the percentage of arable land and to plant composition in the field margin. In addition, our results showed that flower visitor community response to specific flower traits was consistent among years. We also found that the composition of insect assemblages responded to the flower colour and flowering onset in the field margin, whereas in the field centre responded to the flower size.
The percentage of arable land had a negative effect on the fruit set of generalist insect pollinated plant species. However, the fruit set was benefited through the increase of availability of flower resources (Chapter 1). The proportion of organically managed land enhanced the fruit set of species of generalist pollination, whereas it did not have an effect on species of specialist pollination. Competition for pollinators could have occurred between the target species and species thriving in plant communities in the immediate vicinity. However, despite the negative effect of local flower cover, the fruit set benefited from nearby legume crops (Chapter 2).
Finally, we evaluated the abundance of bees and other flower visitors, and the fruit set of two insect-pollinated target plants on the margins of oilseed rape crops and cereal fields in landscapes varying in their landscape structure, as measured by the length of the field-margin network (Chapter 4). Our results showed that the abundance of bees was enhanced by oilseed rape crops, but decreased in complex landscapes (high density of field margin network). On the other hand, the abundance of non-bee flower visitors depended on the landscape structure, particularly on the location of cereal fields. Despite the numerous and diverse communities of flower visitors attracted by oilseed rape crops and wildflower resources, fruit set was enhanced only for the species of generalist pollination, because
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competition processes for flower visitors affect the species of specialist pollination.
Our results highlight the importance of developing agri-environmental schemes that prevent landscape simplification, deploy organic agriculture, include crops that offer flower resources and preserve field margins. These measures may increase the presence of a diverse community flower visitors, which in turn can help to maintain or increase fruit sets in agricultural landscapes.
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Intensificación agrícola, biodiversidad y servicios ecosistémicos
La agricultura es la actividad humana que ocupa la mayor proporción de uso
de la tierra, extendiéndose en casi un 38% de la superficie terrestre (Food
and Agriculture Organization of the United Nations, 2015), y de la que
depende en mayor medida la provisión de alimentos. Sin embargo, la
agricultura es también la principal fuente de gases invernadero, de la
contaminación agroquímica y de la degradación del suelo (Matson, Parton,
Power, & Swift, 1997). Aunado a ello, se considera una de las principales
causas de la pérdida de biodiversidad (Matson et al., 1997; Tilman et al.,
2001), así como de los servicios ecosistémicos asociados (Kleijn et al.,
2009). En particular, la intensificación agrícola se correlaciona con el declive
de los polinizadores y, por ende, con los servicios de polinización que estos
proveen, tanto a los cultivos como a las especies que habitan en los hábitats
naturales y seminaturales no cultivados (Biesmeijer et al., 2006; Potts et al.,
2010; Steffan-Dewenter, Potts, Packer, & Ghazoul, 2005).
La intensificación agrícola ha generado cambios tanto a nivel de
campo como de paisaje en los sistemas agrícolas (Tscharntke, Klein, Kruess,
Steffan-Dewenter, & Thies, 2005). A nivel de campo, se produce
principalmente a través de la gestión de los cultivos. El modelo de gestión
dominante ha sido denominado agricultura convencional, la cual está
caracterizada por el laboreo intensivo, la simplificación en las rotaciones, así
como la aplicación reiterada y profusa de pesticidas (fundamentalmente
herbicidas e insecticidas) y fertilizantes químicos. Además, la
especialización en la producción y la consecuente reducción de los tipos de
cultivos ha promovido una baja diversidad cultivada (Matson et al., 1997),
tanto en el tiempo como en el espacio. Por otro lado, la intensificación ha
impulsado la concentración parcelaria, que genera la agregación de los
INTRODUCCIÓN
10
campos y, por lo tanto, un incremento en su tamaño (Kleijn & Sutherland,
2003). Como consecuencia, todos los hábitats asociados a los campos, como
los que constituyen los márgenes de los mismos, se reducen y simplifican.
Esta reducción y fragmentación de los hábitats naturales y seminaturales, en
conjunto con la escasez de variabilidad espacial y temporal en los usos del
suelo, finalmente causan la homogeneización del paisaje (Tscharntke et al.,
2005).
En España, se destina alrededor de un 34% de la superficie terrestre a
las tierras arables, de las cuales un 41,2% (7.011.097 ha) son cultivos
herbáceos extensivos de secano (Fig. 1; Ministerio de Agricultura y Pesca,
Alimentación y Medio Ambiente, 2016). Estos cultivos de secano están
ampliamente distribuidos en todo el territorio, por lo que su manejo, en
términos de la producción del cultivo y la conservación de los recursos
naturales, resulta fundamental en los sistemas agrícolas. En particular, en
Cataluña los cultivos herbáceos de secano ocupan alrededor de un 38%
(317.294 ha) del total destinado a las tierras arables (835.012 ha) (Fig.1;
Ministerio de Agricultura y Pesca, Alimentación y Medio Ambiente, 2016).
En general, la agricultura de secano se caracteriza por no recibir ningún tipo
de irrigación externa, por lo que dependen del agua obtenida de forma
natural. En los paisajes mediterráneos con cultivos de secano, los bajos
niveles de precipitación son el principal factor que afecta su rendimiento
(Armengot, José-María, Chamorro, & Sans, 2013). Sin embargo, la
biodiversidad asociada a estos paisajes es afectada mayormente por las
técnicas de manejo. Es decir, el uso recurrente de herbicidas y la reducción
de las áreas no cultivadas, como son los márgenes de los campos, han
causado un declive en la diversidad vegetal (Bassa, Chamorro, José-María,
Blanco-Moreno, & Sans, 2012). A diferencia de otros paisajes agrícolas
europeos, los sistemas arables mediterráneos están concentrados en llanuras
no muy extensas delimitadas por una compleja red de comunidades
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vegetales, tales como pastos anuales y perennes, matorrales y bosques. En
este sentido, la pérdida de diversidad vegetal puede causar una disrupción de
los procesos ecosistémicos, como es la polinización, afectando de esta
manera la reproducción de las plantas. En consecuencia, otros componentes
de los agroecosistemas también pueden verse afectados.
La proporción de cultivos herbáceos extensivos se ha utilizado
frecuentemente como un indicador de la intensificación del paisaje. Esta
variable se puede correlacionar con otros atributos del paisaje agrícola como,
por ejemplo, la diversidad y la fragmentación de los hábitats y la densidad de
márgenes. Sin embargo, en los paisajes mediterráneos estudiados, los
cultivos herbáceos extensivos constituyen el uso del suelo mayoritario, por lo
que la proporción de tierra arable (PAL, por sus siglas en inglés) puede ser
utilizada como un indicador de la complejidad del paisaje, en tanto que es
complementario al porcentaje de tierra con hábitats naturales y
Figura 1. Distribución de los principales tipos de cubiertas del suelo en España (panel izquierdo; modificado de Comisión Europea, 2017) y Cataluña (panel derecho; tomado de Ibàñez i Martí & Burriel Moreno, 2010).
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seminaturales. En los sistemas agrícolas mediterráneos se ha demostrado que
la complejidad del paisaje afecta la riqueza y la composición de la flora, y
que además es importante en los márgenes y en los bordes, pero que su
importancia es mucho menor en el interior de los campos (Armengot, José-
María, Blanco-Moreno, Romero-Puente, & Sans, 2011; José-María,
Armengot, Blanco-Moreno, Bassa, & Sans, 2010). Sin embargo, la literatura
relacionada con el efecto de la complejidad del paisaje sobre la abundancia
de los visitantes florales y la provisión de la polinización en los paisajes
agrícolas continúa siendo insuficiente. A partir de este conocimiento, se
podrían desarrollar esquemas de gestión que permitan conservar e incentivar
la biodiversidad, así como restaurar las funciones ecosistémicas, con el fin de
mejorar la sostenibilidad en los sistemas agrícolas.
Los esquemas agroambientales como instrumento para la restauración
del paisaje
En Europa se han adoptado diversas políticas agrarias con el objetivo de
contrarrestar y reducir los efectos negativos que causan las prácticas
agrícolas modernas sobre el medio ambiente (Kleijn & Sutherland, 2003).
Entre las políticas más importantes implementadas para preservar el medio
ambiente y mitigar la pérdida de biodiversidad se cuentan los esquemas
agroambientales. Todos los países que conforman la Unión Europea están
comprometidos a desarrollar e implementar dichos esquemas, impulsándolos
mediante incentivos monetarios destinados a los agricultores (Kleijn &
Sutherland, 2003). La agricultura ecológica es considerada una práctica
agrícola respetuosa con el medio ambiente y forma parte de los esquemas
agroambientales [Reglamento (CE) Nº 834/2007]. Habitualmente se
contrapone a un modelo más o menos estereotipado de la agricultura, que,
aunque heterogéneo, comprende el conjunto de prácticas más extendido, por
13
lo que se lo denomina agricultura convencional. La agricultura ecológica se
diferencia de la agricultura convencional por la rotación de cultivos, la
prohibición de fertilizantes químicos y de pesticidas sintéticos, así como por
la incorporación de abonos verdes y abonos de origen animal a las tierras de
cultivo (Reganold & Wachter, 2016). La agricultura ecológica favorece, a
través de la compleja red de interacciones bióticas que se promueven
mediante las estrategias de manejo, la fertilidad del suelo, el incremento del
uso de recursos internos, la conservación de la biodiversidad y la producción
de alimentos de calidad para el consumo humano y animal (Fig. 2; Stockdale
et al., 2001).
Uno de los objetivos más relevantes planteados por la Comisión
Europea, a través del “Plan de acción para el futuro de la producción
ecológica de la Unión Europea”, es la expansión de la agricultura ecológica.
En la actualidad, se estima que la agricultura ecológica abarca alrededor del
Figura 2. Diagrama del funcionamiento de las bases y estrategias de manejo en la agricultura ecológica (modificado de Reganold & Wachter, 2016).
14
1% de la superficie agrícola mundial y, en particular, en España ocupa el
7,9% (Willer & Lernoud, 2017). Cataluña es la tercera Comunidad
Autónoma con el mayor porcentaje de agricultura ecológica (8,52% en el año
2016), a la que se destinan aproximadamente 171.937 ha (CCPAE, 2016). En
la última década, la superficie agrícola ecológica de Cataluña se ha triplicado
y, con ello, se ha incrementado la producción de cultivos ecológicos como
los cereales y las leguminosas. Sin embargo, el objetivo propuesto por la
Comisión Europea no es exclusivamente impulsar la producción, sino que
también pueda actuar como medida para la conservación de la biodiversidad
en los sistemas agrícolas.
Numerosos estudios han demostrado los efectos positivos de la
agricultura ecológica sobre la riqueza y la abundancia de la flora que
coloniza los campos y los hábitats adyacentes, en comparación con la
agricultura convencional. La alta concentración de recursos florales en los
campos ecológicos estimula la abundancia y la diversidad de polinizadores
(Holzschuh, Steffan-Dewenter, & Tscharntke, 2008; Rundlöf, Nilsson, &
Smith, 2008). Asimismo, se ha demostrado que los beneficios de la
agricultura ecológica dependen de la heterogeneidad del paisaje (Batáry,
Báldi, Kleijn, & Tscharntke, 2011; Rundlöf & Smith, 2006). Por ejemplo,
Holzschuh et al. (2007) evaluaron el efecto de las prácticas ecológicas sobre
la diversidad de abejas, y mostraron que el beneficio aportado por estas
prácticas es más importante en paisajes homogéneos, con un alto porcentaje
de tierra agrícola, que en aquellos más heterogéneos. En este sentido,
determinadas medidas agroambientales pueden resultar más beneficiosas en
paisajes simples, con una baja proporción de hábitats seminaturales, que en
paisajes complejos, con una alta proporción de dichos hábitats (Kleijn,
Rundlöf, Scheper, Smith, & Tscharntke, 2011).
En muchos paisajes agrícolas, la producción está concentrada en
cultivos que no requieren de la actividad polinizadora de los insectos, como
15
son los cereales, lo que puede comprometer el servicio ecosistémico de la
polinización en los hábitats circundantes o en aquellos cultivos minoritarios
que la requieran para su desarrollo. En este contexto, la agricultura ecológica
puede beneficiar a los polinizadores a través de la provisión de recursos
florales, ya que la baja intensidad de la gestión permite que, incluso los
cultivos de cereales, alberguen una flora más diversa y con numerosas
especies entomófilas (Chamorro, Masalles, & Sans, 2016).
La agricultura ecológica también contribuye con el incremento de la
diversidad espacio-temporal de los paisajes agrícolas a través de la rotación
de cultivos. A pesar de que las rotaciones están orientadas principalmente
hacia el rendimiento y la estabilidad de los cultivos (Seufert & Ramankutty,
2017), algunos de los cultivos que se intercalan en las rotaciones de zonas
cerealistas proveen altas concentraciones de recursos florales que pueden
incrementar la abundancia de los polinizadores (Klein et al., 2007). Algunos
de los tipos de cultivos que se incluyen en las rotaciones son leguminosas,
por su alta capacidad fijadora de nitrógeno, y cultivos de floración masiva,
como puede ser la colza (Brassica napus). Esta última, cuyo cultivo se ha
extendido recientemente por la actual demanda de aceite y biocombustible,
ofrece cuantiosas recompensas de polen y néctar como atractivo para los
polinizadores (Morandin & Winston, 2005). Diversos estudios han
demostrado el efecto positivo que tienen los cultivos de floración masiva
sobre los polinizadores, especialmente sobre las abejas (Holzschuh,
Dormann, Tscharntke, & Steffan-Dewenter, 2013; Westphal, Steffan-
Dewenter, & Tscharntke, 2009). Sin embargo, todos ellos también coinciden
en que los beneficios que ofrecen estos cultivos dependen de la presencia de
hábitats naturales y seminaturales en los paisajes agrícolas. A pesar de ello,
los cultivos de floración masiva también pueden influenciar los patrones de
los polinizadores en los hábitats circundantes (Montero-Castaño, Ortiz-
Sánchez, & Vilà, 2016). La mayoría de estos estudios han sido realizados en
16
paisajes centro-europeos; no obstante, existe poca información acerca del
efecto que pueden tener los cultivos de floración masiva sobre la
biodiversidad en paisajes cerealistas mediterráneos altamente intensificados.
Otro factor que puede afectar la magnitud de los efectos de la
agricultura ecológica sobre la biodiversidad es la escala en la que se
implementen estas prácticas (Bengtsson, Ahnström, & Weibull, 2005). Por
ejemplo, la agregación de campos ecológicos en el paisaje puede incrementar
la riqueza y abundancia de los polinizadores (Holzschuh et al., 2008). Por
estas razones son fundamentales la inclusión y la evaluación de los efectos a
múltiples niveles espaciales para comprender los patrones de la biodiversidad
en los sistemas agrícolas, lo que permitirá implementar adecuadamente los
esquemas agroambientales.
La comunidad vegetal, sus atributos funcionales y los visitantes florales
en los sistemas agrícolas
Los cambios que se producen en la estructura del paisaje por la
intensificación agrícola afectan tanto la composición florística de los hábitats
como la composición de los visitantes florales, modificando a su vez la
interacción planta-polinizador a nivel de individuo, población y comunidad
(Kremen et al., 2007). Aunque se suele considerar la interacción entre
plantas y polinizadores como un proceso más o menos unívoco, el contexto
en el que se desarrollan estas interacciones puede ser determinante. Por
ejemplo, los cambios en la estructura del paisaje pueden causar una dilución
o concentración de los visitantes florales, lo cual finalmente altera su
interacción con la comunidad vegetal (Montero-Castaño et al., 2016;
Tscharntke et al., 2012). Además, la comunidad vegetal circundante puede
afectar las interacciones entre cualquier especie de planta y su conjunto de
visitantes florales, reduciendo la tasa de visitas mediante competencia
17
(Pleasants, 1981) o incrementándola a través del proceso de facilitación
(Moeller, 2004).
Estos cambios en la comunidad vegetal, además de generar posibles
repercusiones en la abundancia de los recursos florales y posible
competencia por los visitantes florales, pueden comportar cambios en el
conjunto de los visitantes florales (Kremen et al., 2007). Dichos cambios,
con frecuencia, están mediados por ciertas cualidades del arreglo floral. En
los últimos años, se han evaluado los cambios en las comunidades vegetales,
mediante el uso de los atributos funcionales, en relación con las prácticas
agrícolas y las condiciones ambientales, así como los efectos de la
comunidad funcional resultante sobre los servicios ecosistémicos prestados
(Wood et al., 2015). Los atributos funcionales se definen como
características fisiológicas, morfológicas o fenotípicas de las especies (Violle
et al., 2007). Estos atributos varían entre especies, y las especies difieren en
sus abundancias, por lo que el funcionamiento de la comunidad puede estar
determinado por la distribución de estos atributos. Una manera de
caracterizar la estructura funcional de las comunidades es promediando el
valor del rasgo de las diferentes especies ("community-weighted mean"
[CWM], Violle et al., 2007).
Los atributos funcionales proporcionan información sobre el papel
que desempeñan las especies en la comunidad y de su respuesta ante las
variaciones ambientales (Cornelissen et al., 2003), lo que permite valorar el
impacto que provocan dichos cambios en la comunidad sobre los procesos
ecosistémicos (Garnier et al., 2004). Para evaluar el impacto de la
intensificación y las prácticas agrícolas, se ha propuesto un marco conceptual
que evalúa la respuesta de las comunidades vegetales a los cambios y cómo
estos afectan las funciones y los servicios ecosistémicos (Fig. 3; Esquema
respuesta-efecto; Lavorel & Garnier, 2002; Suding et al., 2008). Por ejemplo,
se ha demostrado que la diversidad de especies vegetales y algunos de sus
18
atributos funcionales (p. ej. formas de vida, área específica foliar) son
afectadas por la intensificación agrícola en paisajes mediterráneos (Guerrero,
Carmona, Morales, Oñate, & Peco, 2014; José-María, Blanco-Moreno,
Armengot, & Sans, 2011; Solé-Senan, Juárez-Escario, Robleño, Conesa, &
Recasens, 2017). Sin embargo, es poco conocido el efecto que tienen los
cambios estructurales de las comunidades vegetales sobre la comunidad de
visitantes florales y sus consecuencias sobre los servicios ecosistémicos que
proveen.
En particular, los atributos visuales de las flores (p. ej. morfología,
color, tamaño, recompensas florales, fenología) pueden determinar la
interacción entre la comunidad vegetal y la comunidad de visitantes florales.
Estos conjuntos de atributos florales, que determinan los denominados
síndromes de polinización, son esenciales en el proceso de atracción, y
pueden ser asociados con visitantes florales específicos (Faegri & Van Der
Pijl, 1979). La mayoría de estudios que relacionan los atributos florales con
la comunidad de visitantes florales se centran en las abejas (Fornoff et al.,
2017), las cuales son consideradas los polinizadores más comunes y de
Figura 3. Marco conceptual que relaciona la respuesta de los atributos a los cambios ambientales y los efectos de estos cambios en el funcionamiento de los ecosistemas (modificado de Suding et al., 2008).
19
mayor valor económico (McGregor, 1976). No obstante, otros visitantes
florales también pueden contribuir con la provisión de los servicios de
polinización en los paisajes agrícolas (Bosch, Retana, & Cerdà, 1997). Se ha
demostrado que la tasa de visitas de otros visitantes florales, en comparación
con las abejas, puede compensar su baja contribución en la deposición de
polen (Rader et al., 2016). Además, los recursos florales que ofrecen los
paisajes agrícolas también benefician a otros visitantes florales (Grass et al.,
2016). Por lo tanto, la incorporación de otros grupos, tales como coleópteros
y dípteros, en el estudio de la comunidad de visitantes florales permite
ampliar nuestro conocimiento acerca de la importancia de la biodiversidad en
la provisión de servicios ecosistémicos en los paisajes agrícolas.
La polinización como servicio ecosistémico
Los cambios que se producen en la comunidad de visitantes florales, tanto en
la abundancia como en la diversidad, pueden afectar la reproducción de las
plantas (Potts et al., 2010). En particular, el declive en los servicios de
polinización puede afectar negativamente a las plantas de polinización
cruzada (Aguilar, Ashworth, Galetto, & Aizen, 2006), siendo más
vulnerables las especies de polinización especializada que aquellas de
polinización generalista (Biesmeijer et al., 2006).
Un amplio porcentaje de estudios han evaluado el potencial servicio
de polinización a través de la abundancia y riqueza de los polinizadores, o
mediante la interacción entre plantas y polinizadores. Sin embargo, la
producción de frutos (fruit set) resulta un enfoque directo para evaluar el
servicio de la polinización. Para ello, se emplean plantas diana o fitómetros,
que se caracterizan por ser auto-incompatibles y polinizadas por insectos
(Woodcock, Pekkola, Dawson, Gadallah, & Kevan, 2014). La auto-
incompatibilidad en estas plantas requiere la interacción con insectos, por lo
20
que la producción de frutos y semillas permite evaluar el éxito de la
polinización (Ghazoul, 2006). Además, el uso de plantas diana o fitómetros
permite evaluar este éxito de la polinización bajo diferentes condiciones
ambientales (Woodcock et al., 2014). Esta metodología ha sido utilizada en
diversos estudios para evaluar el efecto de las prácticas agrícolas,
principalmente aquellas asociadas a los sistemas ecológicos, sobre la
polinización (Brittain, Bommarco, Vighi, Settele, & Potts, 2010; Hardman,
Norris, Nevard, Hughes, & Potts, 2016; Power & Stout, 2011). A pesar de
que el uso de esta metodología se ha ampliado en los últimos años, todos los
estudios se han enfocado en la evaluación de especies de polinización
generalista, sin considerar las diferencias existentes en el grado de
especialización en las interacciones entre las flores y los visitantes florales
(Johnson & Steiner, 2000). Mediante la inclusión de diferentes síndromes de
polinización, se puede evaluar la dependencia de los efectos, que son
causados por los cambios en el paisaje, a la composición del conjunto de
visitantes florales de cada especie de planta.
En los últimos años, se han dedicado numerosos esfuerzos para
intentar comprender las causas de la pérdida de biodiversidad en los sistemas
agrícolas, no solo por su valor intrínseco de conservación y las repercusiones
que pudiera implicar para el funcionamiento de los hábitats naturales, sino
por la dependencia de muchos cultivos con respecto a los visitantes florales
(Kremen, Williams, & Thorp, 2002). Por estas razones resulta fundamental,
en el contexto actual de los sistemas agrícolas, el estudio a diferentes niveles
de los efectos de la intensificación agrícola sobre los visitantes florales y
sobre la polinización. Asimismo, es necesario evaluar los efectos que tienen
las diferentes facetas de la gestión agrícola a todos los niveles, desde el de
paisaje al de campo, y sus consecuencias directas e indirectas sobre la
biodiversidad en los sistemas agrícolas, particularmente en los paisajes
cerealistas mediterráneos.
21
El objetivo general de esta tesis es el estudio del funcionamiento de la
polinización en los paisajes agrícolas mediterráneos dominados por los
cultivos herbáceos extensivos. Para la consecución de este objetivo general,
se evaluó la abundancia y la composición de los principales grupos de
visitantes florales y la producción de frutos de especies diana con diferentes
grados de especialización en la polinización (generalista vs. especialista). La
experimentación fue realizada en paisajes estructuralmente contrastados y
bajo diferentes sistemas de gestión y tipos de cultivos.
A continuación, se detallan los objetivos específicos de cada uno de
los capítulos que conforman la tesis doctoral:
Capítulo 1:
- Estudiar el efecto de la intensificación agrícola a nivel de paisaje
(PAL), de la intensidad de gestión (ecológica vs. convencional), del
tipo de cultivo (cereal vs. leguminosa) y de la distancia al margen
(margen vs. centro), sobre la abundancia de los visitantes florales
(apoideos, coleópteros y dípteros) y sobre la producción de frutos de
la especie diana Raphanus sativus.
- Determinar el efecto de los recursos florales localizados en el margen
y en el centro de campos sobre la abundancia de los visitantes
florales y sobre la producción de frutos de la especie diana Raphanus
sativus.
Capítulo 2:
- Estudiar el efecto de la proporción de tierra arable bajo gestión
ecológica a nivel de paisaje sobre la abundancia de abejas (apoideos)
OBJETIVOS
22
y sobre la producción de frutos de las especies diana Raphanus
sativus y Onobrychis viciifolia con diferente grado de especialización
en su interacción con los polinizadores.
- Evaluar el efecto de la intensidad de gestión (ecológica vs.
convencional) y del tipo de cultivo (cereal vs. leguminosa), así como
el efecto de los recursos florales localizados en los márgenes sobre la
abundancia de abejas (apoideos) y la producción de frutos de las
especies diana Raphanus sativus y Onobrychis viciifolia.
Capítulo 3:
- Evaluar los cambios en la composición florística, sus atributos
florales y la composición de familias de los visitantes florales
(apoideos, coleópteros y dípteros) de los márgenes de los cultivos
herbáceos extensivos de secano en relación con la intensificación
agrícola (PAL) a nivel de paisaje, la intensidad de gestión (ecológico
vs. convencional), el tipo de cultivo (cereal vs. leguminosa) y la
distancia al margen del campo (centro vs. margen).
- Estudiar la relación entre la composición florística y la composición
de familias de los visitantes florales (apoideos, coleópteros y
dípteros), así como la relación entre la comunidad de visitantes
florales y los atributos florales de la comunidad vegetal.
Capítulo 4:
- Analizar el efecto de la estructura del paisaje (densidad de márgenes)
y de la presencia de cultivos de floración masiva (cultivo de colza)
sobre la abundancia de abejas (apoideos) y otros visitantes florales
(coleópteros, dípteros y otros himenópteros), así como sobre la
23
producción de frutos de las especies diana Raphanus sativus y
Onobrychis viciifolia en paisajes caracterizados por un alto
porcentaje de tierra agrícola.
- Analizar el efecto de los recursos florales a nivel de parcela sobre la
abundancia de abejas (apoideos) y otros visitantes florales
(coleópteros, dípteros y otros himenópteros), así como sobre la
producción de frutos de las especies diana Raphanus sativus y
Onobrychis viciifolia.
24
En cada uno de los capítulos se exponen todos los materiales y métodos de
forma detallada y sus respectivas referencias. Sin embargo, a continuación se
describe de manera abreviada la metodología general utilizada en esta tesis
doctoral.
Área de estudio
Los estudios se llevaron a cabo durante los años 2013 (Capítulos 1 y 3), 2014
(Capítulo 4) y 2015 (Capítulos 2 y 3) en Cataluña, al noreste de España
(Fig. 4). La zona de estudio, concentrada principalmente en la Depresión
Central Catalana, presenta un clima mediterráneo con una precipitación
media anual que oscila entre los 350 y los 850 mm, y una temperatura media
anual que varía entre los 11 y los 14ºC. Las localidades de muestreo se
ubicaron en las comarcas de Anoia, Bages, Berguedà, Moianès, Osona,
Segarra, Solsonès y Vallès Oriental.
Para el diseño experimental del capítulo 1, se seleccionaron 10
localidades que diferían en la complejidad del paisaje, obteniendo un
gradiente en el uso de tierra agrícola. Para ello, se midió el porcentaje de
tierra arable (PAL, por sus siglas en inglés), en áreas circulares de 1 km de
radio. Los valores del PAL variaron entre el 20%, que representaron los
paisajes complejos, y el 80%, que representaron los paisajes simples. En
cada localidad, se seleccionaron campos que diferían en el nivel de
intensidad de manejo (ecológico vs. convencional) y en el tipo de cultivo
(cereal vs. leguminosa). En los campos de cereales, se evaluaron dos
posiciones: centro y margen, mientras que en los campos de leguminosas
únicamente se evaluó el centro (Fig. 5a). Para el diseño experimental del
capítulo 2, se seleccionaron cinco localidades que diferían en la proporción
de tierra arable bajo manejo ecológico (POL), estimada como la relación
entre el área agrícola bajo manejo ecológico respecto al área de tierra arable.
METODOLOGÍA
25
Dicha proporción fue calculada en áreas circulares de 500 m de radio, y varió
entre 0,2 y 79,6%. En cada localidad, se seleccionaron campos con diferente
manejo (ecológico vs. convencional) y tipo de cultivo (cereal vs.
leguminosa), en los que se muestreó el margen del campo (Fig. 5b). El
diseño experimental del capítulo 3 corresponde con lo expuesto para los
capítulos 1 y 2 (Fig. 5a y 5b), con la variante de que en ambos casos el PAL
se calculó a una escala común de 500 m de radio. Finalmente, para el diseño
experimental del capítulo 4, se seleccionaron 21 márgenes entre campos de
colza (cultivo de floración masiva) y campos de cereales, y 21 márgenes
entre campos de cereales, en un área con un PAL mayor del 75% (Fig. 5c).
Se evaluó la estructura del paisaje mediante la densidad de hábitats no
cultivados en áreas circulares de 500 m de radio; la suma total de estos
elementos lineares del paisaje varió entre 6,64 y 28,52 km.
Figura 4. Ubicación de las localidades muestreadas en cada diseño experimental en Cataluña, España. Las localidades seleccionadas en el año 2013 están simbolizadas por triángulos, las del año 2014 por un rectángulo y las del año 2015 por cuadrados (Modificado del ICGC, 2015).
26
Figura 5. Esquema de cada diseño experimental: (a) Capítulos 1 y 3, (b) Capítulos 2 y 3, y (c) Capítulo 4.
(a)
(b)
(c)
27
Recursos florales
En los campos seleccionados en cada año se evaluó la riqueza y la
abundancia de las especies en flor (Fig. 6). Solo fueron consideradas aquellas
especies polinizadas por insectos. Para ello, se realizaron transectos paralelos
al margen en el centro (Capítulos 1 y 3), margen y borde de los campos
(Capítulos 1-4). Cada muestreo se realizó una vez por semana durante cinco
o seis semanas, y se contabilizó el número de flores abiertas o la cobertura de
las plantas en flor en el transecto, según el diseño experimental. En el caso
de la cobertura, esta fue estimada visualmente. Todas las plantas
contabilizadas en los transectos fueron identificadas a nivel de especie. La
nomenclatura de las especies sigue de Bolòs et al. (2005).
Visitantes florales
Para evaluar la abundancia de los visitantes florales en cada muestreo, se
utilizaron los platos-trampa (pan traps), localizados en el centro (Capítulos 1
y 3) y en el margen (Capítulos 1-4) de cada campo seleccionado. Estas
trampas están compuestas por tres recipientes (500 mL, 160 mm diámetro)
pintados de color azul, amarillo y blanco, con un esmalte sintético que refleja
la luz ultravioleta (Fig. 7). Las trampas fueron colocadas 1 m por encima del
suelo y separadas 1 m de cada grupo de plantas diana, y permanecieron
activas durante un período de 12 o 24 horas (esta diferencia en exposición
apenas afecta el volumen de capturas, ya que estas trampas son efectivas para
visitantes florales diurnos). Los recipientes que componen las trampas fueron
llenados con agua y una pequeña cantidad de jabón, para reducir la tensión
superficial. Los muestreos se realizaron en días soleados bajo condiciones
favorables de temperatura (>18 °C) y de baja velocidad del viento,
coincidiendo con los muestreos de los recursos florales. Los especímenes
colectados fueron almacenados en alcohol etílico al 70% y, posteriormente,
28
identificados a nivel de familia (únicamente himenópteros, coleópteros y
dípteros).
Figura 6. Foto de detalle de los recursos florales, en donde se señala el centro, el borde y el margen del campo.
Figura 7. Fotos de detalle de los platos-trampa, empleados para la captura de los visitantes florales.
29
Especies diana y producción de frutos
Se seleccionaron Raphanus sativus L. (Brassicaceae) y Onobrychis viciifolia
Scop. (Fabaceae) como especies diana, para evaluar la producción de frutos.
Raphanus sativus es una planta anual que produce numerosas flores
actinomorfas de color blanco o blanco-rosáceo, dispuestas en inflorescencias
racemosas. Es una especie autoincompatible (Young & Stanton, 1990) y
visitada por diversos tipos de polinizadores, tales como abejas, abejorros,
abejas silvestres, sírfidos y mariposas (Albrecht, Duelli, Müller, Kleijn, &
Schmid, 2007; Steffan-Dewenter & Tscharntke, 1999). Onobrychis viciifolia
es una especie perenne que produce numerosas flores papilionadas de color
rosado (Kells, 2001). Se caracteriza por presentar polinización entomófila
obligada (Hanley et al., 2008), particularmente por abejas, abejorros y abejas
silvestres (Hayot Carbonero, Mueller-Harvey, Brown, & Smith, 2011). De
acuerdo con la morfología que presentan las flores, se clasificaron como
especies con diferentes grados de especialización en la polinización, R.
sativus como generalista y O. viciifolia como especialista (Fig. 8).
Figura 8. Fotos de detalle de las especies diana en floración: (a) Raphanus sativus y (b) Onobrychis viciifolia.
(a) (b)
30
Para la evaluación de la producción de frutos, se sembraron semillas
de cada especie en macetas de 5 L con suelo comercial (mezcla de turba,
vermiculita y arcilla). Las macetas fueron colocadas en espacios abiertos en
los Campos Experimentales de la Universidad de Barcelona, bajo
condiciones controladas de riego. Previo al inicio de la floración, los
individuos de cada especie diana fueron trasladados a los campos
seleccionados, agrupados por especies y colocados a cada lado de los platos-
trampa. En el diseño experimental del Capítulo 1 se utilizaron cuatro
individuos de la especie diana R. sativus por campo y posición, para el
Capítulo 2 se utilizaron ocho individuos de cada especie diana (R. sativus y
O. viciifolia) por campo, y para el Capítulo 4 se utilizaron seis individuos de
cada especie diana (R. sativus y O. viciifolia) por margen. Una vez concluido
el período experimental (cinco o seis semanas entre los meses de abril y
junio), los individuos fueron trasladados de vuelta a los invernaderos en los
Campos Experimentales para evitar el contacto de las plantas con cualquier
potencial polinizador. Todos los individuos se mantuvieron bajo riego
periódico durante dos semanas para permitir el desarrollo de los frutos.
Asimismo, durante dicho período se eliminaron los brotes florales, para
evitar la sobreestimación de flores no polinizadas durante el período
experimental. Finalmente, para calcular la producción de frutos se
contabilizaron todos los frutos bien desarrollados y el número de flores que
no fueron polinizadas.
CAPÍTULOS
CAPÍTULO 1
Agricultural landscape structure and field management have contrasting effects on the community of flower visiting insects and on the fruit set of target plants José M. Blanco-Moreno, Marian Mendoza-García, Laura Armengot, Paola Baldivieso-Freitas, Berta Caballero-López, Lourdes Chamorro, Laura José-María, Roser Rotchés-Ribalta, F. Xavier Sans En fase de preparación para su envío a Journal of Applied Ecology
CAPÍTULO 1
35
1. Management intensification at different levels is one of the main causes of
biodiversity decline in agricultural landscapes. Organic farming, as well as
increasing availability of flower resources in the landscape, is proposed to
counteract these negative effects on the community of flower visitors in
agroecosystems. However, the effects of these environmental measures on
the ensemble of flower visiting insects, and on the delivery of pollination
services, are not fully understood.
2. We selected fields with different level of management intensity (organic
vs. conventional) and crop type (cereal vs. legume) in ten localities across a
gradient in agricultural land use (percentage of arable land, PAL). In each
field, we placed pan traps and a set of insect pollinated target plant species of
generalist pollination (Raphanus sativus). We analysed the effect of PAL,
management, position and crop type and the effects of availability of flower
resources on flower visitor abundance and on the fruit set of the target plant.
3. PAL affected negatively the abundance of flower-visiting insects, although
this effect was not consistent among the groups of flower visitors (positive
for Apoidea and Coleoptera). Field margins always hosted higher
abundances than centres. Organic farming at field level had a positive effect
on the overall abundance of flower visitors; moreover, it smoothed the
effects of landscape and position within the field. The effect of legumes was
not significant on the abundance of flower visitors, except for flower-visiting
beetles.
4. PAL had a negative effect on the fruit set of the target plant. The fruit set
was benefited through the increase of availability of flower resources in
organic crops, crop margins and in legume crops.
SUMMARY
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36
5. Synthesis and applications. Flower visitor abundance and fruit set were
strongly affected by PAL and flower resources, suggesting that the
prevention of landscape simplification, the promotion of organic farming, the
conservation of field margins and the increment of flower resources at the
field level may enhance the presence of a diverse community flower visitors
in agricultural landscapes, which in turn can help to the maintenance of
pollination services.
Keywords: Agricultural intensification, agroecosystems, flower resources,
flower visitors, pollination services, organic farming, field margins
CAPÍTULO 1
37
Flower-visiting insects have undergone recent declines (Biesmeijer et al.,
2006; Garibaldi, Aizen, Cunningham, & Klein, 2009; Tscharntke, Klein,
Kruess, Steffan-Dewenter, & Thies, 2005), which have raised academic and
public concern about cascading effects on pollination delivery (Andersson,
Rundlöf, & Smith, 2012; Kremen, Williams, & Thorp, 2002; Pires et al.,
2014; although see Kleijn et al., 2015) with potential enormous economic
consequences (Gallai, Salles, Settele, & Vaissière, 2009; Vanbergen et al.,
2013). Agricultural intensification is one of the major causes for biodiversity
loss in agricultural landscapes (Kleijn et al., 2009; Krebs, Wilson, Bradbury,
& Siriwardena, 1999) and thus it is sensible to find management options that
reconcile production with biodiversity conservation. However, agricultural
intensification is compounded by several processes acting at different levels.
At landscape level, it is the result of the suppression and degradation of
natural and seminatural habitats, as well as reducing crop diversity and crop
rotation simplification. At field level, agricultural intensity relates to the
effectiveness with which agricultural practices are implemented and to the
amount of external inputs, which translate into an ecological
oversimplification. Both facets of intensification have been shown to have
negative effects on biodiversity (Andersson, Birkhofer, Rundlöf, & Smith,
2013; José-María, Armengot, Blanco-Moreno, Bassa, & Sans, 2010) and can
also affect associated ecosystem services (Andersson et al., 2012; Tilman et
al., 2001).
Insect abundance is negatively affected by the management of
agricultural landscapes. On the one hand, the reduction of non-crop habitats
entails an oversimplification of the landscape, as field margins are often
suppressed or much reduced (Tscharntke et al., 2005). In fact, in very
intensively managed landscapes, field margins can be the only remnants of
seminatural vegetation, and constitute the refuge for many plant and animal
INTRODUCTION
CAPÍTULO 1
38
species (Fahrig et al., 2011; Marshall & Moonen, 2002; Meek et al., 2002;
Rands & Whitney, 2011), as well as their main corridors in agricultural
landscapes (Hass et al., 2018). On the other hand, homogeneous
monoculture, and particularly that of cereals, narrows the habitat choices and
reduces the opportunities for flower visiting insects (Nicholls & Altieri,
2013).
Organic farming is known to counteract the negative effects exerted
by agricultural management on many components of agroecosystems’
biodiversity, both within fields and on the neighbouring habitats (Bassa,
Chamorro, José-María, Blanco-Moreno, & Sans, 2012; Bengtsson,
Ahnström, & Weibull, 2005; José-María et al., 2010; Rundlöf, Bengtsson, &
Smith, 2008). Organic farming differs from conventional farming in several
key aspects which altogether define a lower farming intensity (Armengot et
al., 2011). Fundamental differences are determined by the prohibition of
most pesticides and inorganic fertilizers (Council of the European Union,
2007), needing thus alternative ways to supplement the crops’ nutrient
requirements, with e.g. legumes which may provide nitrogen through
fixation from atmosphere (Crews & Peoples, 2004; Pe’er et al., 2017). Both
aspects usually entail an increased within and among field heterogeneity and
boost flower abundance and diversity compared to conventional
management. The enhancement of plant communities broadens the
opportunities for different organisms. These differences in relation to the
common practice in conventional agriculture benefit the biodiversity of
several taxonomic groups, though the effects are not always consistent
(Caballero-López et al., 2011; Gabriel & Tscharntke, 2007; José-María et al.,
2010; Kennedy et al., 2013; Puech, Baudry, Joannon, Poggi, & Aviron,
2014; Rundlöf & Smith, 2006; Smith, Dänhardt, Lindström, & Rundlöf,
2010).
CAPÍTULO 1
39
Although many major staple crops such as cereals do not depend on
pollinators, and offer very scant resources for them, these crops occupy
substantial areas all over Europe. About a 40 % of the land is devoted to
agriculture and about 33.2 % of it is annually tilled land devoted to cereals
(Eurostat, 2013). However, these crops alternate either in time or space with
insect-pollinated crops. These crops, like the legume crops that are routinely
included in organic crop rotations, may benefit from the presence of flower
visiting insects, but at the same time they may also influence the activity of
the insects. Also, in agricultural landscapes, these crops are intermixed with
the remnants of seminatural and natural habitats, where some plant species
may require the interaction with insects to produce fruits and viable seed
(Andersson, Ekroos, Stjernman, Rundlöf, & Smith, 2014; Bartomeus, Vilà,
& Steffan-Dewenter, 2010; Biesmeijer et al., 2006). Thus, it is necessary to
understand how the ensemble of flower visiting insects responds to
landscape structure and crop characteristics and management, and how does
their response affect the fruit set of insect-pollinated plants. Different groups
of insects interact with entomophilous flowers, and although they display
very different efficiencies as pollinators, it is considered that some can
compensate their low efficacy through increased frequency of visits (Power,
Jackson, & Stout, 2016; Rader et al., 2016).
However, it is equally important to understand the cascading effects
on plant reproduction, if research aims to provide with meaningful
recommendations at the whole agroecosystem level. The link between the
abundance of flower visiting insects and the fruit or seed set of target plants
has been investigated previously, generally supporting that the measures that
favour flower visiting insects, and particularly bees, increase fruit set
(Hardman, Norris, Nevard, Hughes, & Potts, 2016; Mendoza-García,
Blanco-Moreno, Chamorro, José-María, & Sans, 2018; Power & Stout,
2011). Nevertheless, it is not clear whether the agricultural landscape and
CAPÍTULO 1
40
crop characteristics affect flower visiting insects and whether these effects
make a strong difference on the fruit set of insect-pollinated plants
(Bartomeus et al., 2014). A better understanding of these links will aid to
enhance flower visiting insects and the delivery of pollination, thus
facilitating the multiple roles that agricultural landscapes can have
(Shackelford et al., 2013).
We investigated the effects of agricultural land use intensity at
different levels on the abundance of flower-visiting insects and on the fruit
set of an insect pollinated target plant. We aimed at answering the following
questions: a) is the abundance of flower-visiting insects negatively affected
by landscape level agricultural intensity? b) do crop margins affect the
abundance of flower-visiting insects? c) can organic farming compensate for
the negative effects of agricultural intensification at landscape level? d) what
is the role of flower-resources, either offered by flower-resource rich crops
such as legumes of by wildflowers in crop margins, on modulating the
effects of agricultural intensification? e) how does the effect of these factors
translate into the pollination service delivered by flower-visiting insects, and
thus into the fruit set of a target plant?
Plant diversity follows a gradient from the high-diversity margins to
the low-diversity centres owing to differences in farming intensity, and this
gradient is steeper in low-intensity landscapes (low percentage of arable
land) than in high intensity landscapes (José-María et al., 2010). These
differences owe to the stronger landscape effects in the margins, while the in-
field management plays a prominent role in the field centres. However, while
this is true for plants, with passive dispersal at short distances, there are few
empirical evidences that insects, and thus the services that they deliver,
respond in the same way, in spite of indirect evidence (Gabriel &
Tscharntke, 2007; José-María, Blanco-Moreno, Armengot, & Sans, 2011)
although recent studies indicate that field margins in fact concentrate most of
CAPÍTULO 1
41
the movement of pollinators (Hass et al., 2018). We hypothesize that
landscape level agricultural intensity should have a negative effect on the
abundance of flower-visiting insects. These effects should be noticeable on
the margins and on the centre of the fields. However, it is known that many
bee species have relatively short-range foraging distances and respond to the
local availability of foraging resources (Rands & Whitney, 2011; Torné-
Noguera et al., 2014), and it is likely to be true for many different groups of
insects (Hof & Bright, 2010; Millán de la Peña, Butet, Delettre, Morant, &
Burel, 2003). Therefore, we hypothesize that distance to the field margins
should have a negative effect on the insect abundance. However, it is not that
management affects directly the insects. Flower visiting insects may be
determined more by the availability of flower resources than by the
management or position within the field (Haaland, Naisbit, & Bersier, 2011).
In relation to the resources offered by a flower-rich crop, such as legume
crops, we hypothesize that this kind of crop could concentrate flower-visiting
insects (Holzschuh, Dormann, Tscharntke, & Steffan-Dewenter, 2011;
Holzschuh, Steffan-Dewenter, & Tscharntke, 2008; Westphal, Steffan-
Dewenter, & Tscharntke, 2003), and therefore these effects may be more
noticeable in high-intensity landscapes. All these effects may translate into
the fruit set of target species, although it is likely that target plants do not
suffer much from pollinator limitation as dominant pollinators persist under
agricultural expansion and may be easily enhanced by means of simple
measures (Kleijn et al., 2015).
CAPÍTULO 1
42
Experimental sites
The study was conducted in 2013 in the dryland cereal region in Catalonia,
NE of Spain (1.56° - 2.21°E, 41.75° - 42.05°N) (Fig. 1). To examine the
dependence of flower-visiting insects on the agricultural landscape we
selected ten localities, defined as non-overlapping areas of 1 km radius, that
were selected to represent a gradient in agricultural land use, measured as the
percentage of arable land (PAL). The set of localities covers an approximate
area of 54 × 34 km. PAL was determined within a 1 km radius of each field
using the land use information available in the digital Catalan Cartography of
Habitats (Carreras & Diego, 2004). To test the effects of within field
agricultural management on the activity-density of flower-visiting insects,
we selected fields with differing level of management intensity, as displayed
by organic and conventional farms (Armengot et al., 2011). The selection of
the localities was limited by the availability of organic farmers who have
applied organic farming for at least 10 years, as there may be some lag
before the effects of agroecological transition are noticeable (Andersson et
al., 2012). In each of these sites we selected a cereal field from an organic
farm and a cereal field from a neighbouring conventional farm. The
conventional field was selected to match the organic one in size and in the
conditions of the surroundings.
To test the effects of increased flower resources offered by crops,
within these cereal dominated landscapes, a legume crop was also selected in
eight of the ten organic farms. It was not possible to find legumes in two of
the organic farms, and the conventional farmers in the area seldom include
legumes in their crop rotations, so only organic legumes were included in the
experimental design. On each of these fields we carried out surveys of flower
resources, insect sampling and pollination measures as described below. The
measurements were taken on the edge of cereal fields and 20 m towards the
MATERIALS AND METHODS
CAPÍTULO 1
43
centre of the field (hereinafter field centre), and in the field centre of the
legume fields. Field edges of legume crops were excluded from the
experimental design to avoid the confounding effects of increased flower
abundance both in-crop and in the field margin.
Figure 1. Map indicating study area within Catalonia (above) and the 10 localities selected in the study area (below). The grey shading indicates topography in 500 m intervals (above) and the percentage cover of agricultural land (PAL) within 1 × 1 km pixels (below). The names and more information on the localities can be found in Table S1.
CAPÍTULO 1
44
Flower resources
We evaluated the abundance of entomophilous plants in bloom during the
sampling periods. All plants were identified to species level (Table S2), and
the abundance of flowers was assessed by counting the number of open
flower units per species. A flower unit was considered a single flower in
most plants, but in Asteraceae and Apiaceae the smallest distinguishable
inflorescence units (heads and partial umbels) were counted. However, as
flower units differ greatly in their size, all flower units were weighed by their
average size, so our estimates of flower abundance are a surrogate of flower
size summed over the whole sample. The surveys were conducted from May
6th to June 25th in three parallel transects of 1 × 10 m in the studied fields.
These transects corresponded to the field margin, the crop edge (first meter
of the crop) and the centre of the field. Margin and crop edge transects were
averaged, as they are in contact and may affect each other.
Flower visitor survey
We measured insect abundance from May 6th to June 25th, covering most of
the flowering period of the vegetation within crops and field margins in the
area. Insect activity-density was measured by means of pan traps. We used
500 mL plastic bowls (Pro’Jet, Paris, France) painted with UV-reflecting
yellow, white, and blue paint (Sparvar Leuchtfarbe, Spray-Color GmbH,
Merzenich, Germany) to maximize their attractiveness to a broad array of
flower-visiting insects. Each trap consisted of three plastic bowls, one of
each colour, filled with water with a drop of detergent, and were located 1 m
above the ground and 1 m apart from the target plants. Pan traps were set up
between 7:00 and 8:00 a.m. and were collected 12 hours later, thus covering
most of the daily activity period. Traps operated simultaneously on all fields,
under fair weather in calm days. Pan trapping is known to underestimate
flower-visiting insect richness (particularly bees) and to provide a very
CAPÍTULO 1
45
indirect measure of flower visitation (Popic, Davila, & Wardle, 2013;
Westphal et al., 2008). However, this method allows to sample all sites
simultaneously, to avoid biases inherent to collectors, and to standardize
sampling effort easily (Torné-Noguera et al., 2014). Insects were identified
to family in the laboratory, and only bees within Hymenoptera (Apoidea
Anthophila in a restricted sense, including: Megachilidae, Apidae,
Mellittidae, Andrenidae, Halictidae and Colletidae), Diptera and Coleoptera
were used in the analyses. Of the latter two orders, we considered only
putative flower-visiting families according to the available literature and
expert criteria (Oosterbroek & Hurkmans, 2006; Willemstein, 1987).
Fruit set measurements
Raphanus sativus L. (Brassicaceae) was used as a phytometer, the target
species on which fruit set was measured. This plant is known to be self-
incompatible and pollinated by insects (Klotz, Kühn, & Durka, 2002; Young
& Stanton, 1990), and therefore it has been used frequently in pollination
experiments as its reproductive success can be related to pollination by
insects (Bartomeus et al., 2010; Dainese, Montecchiari, Sitzia, Sigura, &
Marini, 2017; Steffan-Dewenter & Tscharntke, 1999). Furthermore, it is
visited by a broad array of insects, which makes it appropriate to measure the
overall effects of flower visitor assemblage on the delivery of pollination
services to it (Albrecht, Duelli, Müller, Kleijn, & Schmid, 2007; Steffan-
Dewenter & Tscharntke, 1999). Plants were grown in 5 L pots at the
Experimental Field Services of the University of Barcelona between January
and May. From May 9th to the 16th potted plants were placed in the studied
fields. One cluster of four plants was placed on each of the selected positions
(either on the edge or the centre of the crop, in conventional and organic
cereal crops as well as in the centre in organic legume fields), at such a
distance between them as to avoid accidental pollination. Plants were
CAPÍTULO 1
46
watered as required (once or twice per week) during the development of the
experiment. On June 25th and 26th, plants were taken back to the
greenhouses at the Experimental Field Services to enable the full
development of recently pollinated flowers. To avoid pollination in the
greenhouse, all remaining and newly developed flower buttons were cut off
periodically for the following two weeks. Fruit set was assessed as the ratio
of ripe fruits to flowers produced. Flowers that develop and blossom can be
counted even if they do not develop into a fruit because their pedicels remain
attached to the inflorescence axes, which allow them to be counted even if
they do not develop into a fruit.
Statistical analyses
We modelled insect abundance by means of generalized mixed effects
models with a Poisson error distribution. We analysed separately the data for
cereals, which allowed testing the effects of management and position, and
the data for organic field centres, which allowed testing the effect of crop.
Two models were used to model total insect abundance and the abundance of
each of the groups considered (Apoidea, Diptera, Coleoptera), which were
compared based on their Akaike information criterion corrected for small
sample sizes (Burnham & Anderson, 2002).
In the first model (Model 1) we included management (conventional
vs. organic), position (edge vs. centre) and crop (cereal vs. legume) as fixed
effect factors, as well as the PAL as a fixed effect covariate.
In the second model (Model 2) we tested whether the differences in
insect abundance could be attributed to differences in the abundance of
flower resources. Given that the abundance of flowers was highly
heterogeneous among localities, and that the effect of varying flower
resources can only affect the local pool of insects (which we hypothesize that
varies from locality to locality in relation to PAL), we log-transformed and
CAPÍTULO 1
47
standardised flower abundance within localities before including it in the
statistical models. We did not include the abundance of flowers as a predictor
in the models with crop and management factors because there is some
collinearity between management and flower resources (there are more
flower resources in legume crops than in cereal crops; in field margins than
in field centres; and in organic fields than in conventional fields; see Fig. S1
and Table S2). Insect abundance was highly variable between localities and
along the sampling period (see supplementary material Fig. S2 and Table
S1). Therefore, all the models included locality as a random effect factor,
plus an uncorrelated random slope for the effect of sampling period between
localities.
Fruit set was modelled as a binomial process by means of generalized
mixed effects models. Since fruit set was measured at the end of the
experiment, a single measure of developed fruits vs. opened flowers per plant
was obtained. For modelling fruit set, we followed a similar strategy as for
insects, and analysed separately the data from cereal fields and from organic
field centres. For each of these subsets of data, we set up three models.
Model 1 considered the effects of landscape, management, and position for
cereal fields, and landscape and crop for organic field centres. Model 2
included the effects of landscape and flower resource abundance. For fruit
set, however, we set up a third model considering the abundances of the
flower visiting insect groups on the fruit set of the target plants. Since
management, position and crop affect flower resources, and these in turn
could affect insect abundance, we decided not to include all three types of
variables in the same model, but, like in the case of insects, we compared the
three models in terms of their Akaike information criterion. For the inclusion
of flower resource abundance and insect abundance (which were measured in
the six sampling periods) in the models of fruit set (which was only
measured at the end of the experiment), we obtained an overall measure for
CAPÍTULO 1
48
flower resources and for the different groups of flower-visiting insects. We
tested the predictive values of the average, the maximum, minimum and
variance of these variables; since there were no significant differences in the
models (and some did not converge, results not shown), we retained the
models including only the average flower resource abundance and the
average insect abundance.
All models were fitted and evaluated by means of package lme4
(Bates, Maechler, Bolker, & Walker, 2015) for R (R Core Team, 2018).
CAPÍTULO 1
49
Flower-visiting insects’ abundance
Overall abundance of flower-visiting insects was found to be affected by the
gradient in agricultural land-use (PAL), by the differences in land-use
intensity and by the distance to field margin (Table 1, Fig. 2a). In general,
despite the consistent positive effect of flower resources on the abundance
across taxonomic groups, their abundances were better explained by Model 1
(including management and position factors), although the differences
between Model 1 and Model 2 were minor.
Flower-visiting insects’ abundance was lower in landscapes
dominated by agricultural land-use than in landscapes with a higher
proportion of non-cropped habitats, and it was also lower in conventional
fields than in organic fields. However, the effect of organic farming was
lower than the effect of landscape (Table 1). Flower-visiting insects
concentrated significantly their activity in field margins compared to field
centres, and this effect was larger than the estimated difference between
organic and conventional fields. This pattern related to the response of
Diptera to the tested variables. However, the positive effect of position
(margin vs. centre) was significant for total abundance, Apoidea and
Coleoptera, but not for Diptera. The interaction between position and
management, as well as between position and PAL were significant, but of
differing direction: whereas at high PAL the difference between margins and
centres increased, under organic farming this difference was reduced.
Nevertheless, PAL by itself had a positive effect on both Apoidea and
Coleoptera abundances.
RESULTS
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Table 1. Effect of the percentage of arable land (PAL), management (organic vs. conventional), position (margin vs. centre), corresponding to the Model 1, and the effect of PAL and the abundance of flower resources, corresponding to the Model 2, on the overall abundance of flower visiting insects and on the abundance of Apoidea, Diptera and Coleoptera. Green entries indicate statistically significant positive effects; red entries statistically significant negative effects and black entries are non-significant effects. On the last row, the Akaike Information Criterion for the best fitting model for each response variable is indicated in bold.
Total abundance Apoidea Model 1 Model 2 Model 1 Model 2
PAL -0.27 ± 0.05*** -0.23 ± 0.04*** 0.72 ± 0.27** 0.64 ± 0.22** Management (M) 0.15 ± 0.03*** 0.37 ± 0.18* Position (P) 0.26 ± 0.03*** 0.61 ± 0.17*** Flower resources (F) 0.16 ± 0.01*** 0.33 ± 0.07*** PAL × M 0.01 ± 0.02 -0.23 ± 0.11* PAL × P 0.04 ± 0.02** 0.21 ± 0.11 M × P -0.22 ± 0.04*** -0.21 ± 0.22 PAL × F 0.01 ± 0.01 0.03 ± 0.07
AICc 4422.25 4306.88 763.34 764.53
Diptera Coleoptera Model 1 Model 2 Model 1 Model 2
PAL -0.76 ± 0.07*** -0.60 ± 0.06*** 0.67 ± 0.10*** 0.46 ± 0.09*** Management (M) 0.15 ± 0.03*** 0.09 ± 0.06 Position (P) 0.02 ± 0.03 0.79 ± 0.05*** Flower resources (F) 0.07 ± 0.01*** 0.34 ± 0.02*** PAL × M 0.07 ± 0.02*** -0.08 ± 0.03** PAL × P 0.06 ± 0.02** -0.07 ± 0.03* M × P -0.40 ± 0.04*** 0.05 ± 0.07 PAL × F -0.05 ± 0.01*** -0.02 ± 0.02
AICc 4354.09 4474.78 2162.65 2443.22 * P<0.05; ** P<0.01; ***P<0.001
For the analysis of overall insect abundance in organic field centres,
Model 1 provided a better fit of the data, and supported a consistent negative
effect of increasing PAL on the abundance of flower visiting insects (Table
2, Fig. 2b). The effect of legume crops on insect abundance, although
positive, was not statistically significant on the overall abundance of insects.
CAPÍTULO 1
51
The three groups of insects displayed a similar pattern, with differences in
the goodness of fit and significance of the explanatory variables (Model 2 for
Diptera should not be considered, as it did not converge to a meaningful
solution, and its fit is much poorer than Model 1). Flower visiting Coleoptera
were more sensitive to crop and flower resource abundance, whereas the
effect of PAL, although also negative, was not statistically significant.
Table 2. Effect of the percentage of arable land (PAL) and crop type (cereal vs. legume), corresponding to the Model 1, and the effect of PAL and the abundance of flower resources, corresponding to the Model 2, on the overall abundance of flower visiting insects and on the abundance of Apoidea, Diptera and Coleoptera. Green entries indicate statistically significant positive effects; red entries statistically significant negative effects and black entries are non-significant effects. On the last row, the Akaike Information Criterion for the best fitting model for each response variable is indicated in bold.
Total abundance Apoidea Model 1 Model 2 Model 1 Model 2
PAL -0.41 ± 0.16* -0.08 ± 0.18 -0.05 ± 0.17 -0.05 ± 0.15 Crop (C) 0.25 ± 0.21 0.26 ± 0.16 Flower resources (F) 0.05 ± 0.08 0.06 ± 0.15 PAL × C -0.08 ± 0.20 0.14 ± 0.14 PAL × F -0.13 ± 0.02*** 0.16 ± 0.11 AICc 1793.66 2389.25 395.89 389.11
Diptera Coleoptera Model 1 Model 2 Model 1 Model 2
PAL -0.08 ± 0.36 0.65 ± 0.17*** -0.02 ± 0.13 -0.15 ± 0.11 Crop (C) 0.23 ± 0.27 0.43 ± 0.10*** Flower resources (F) 0.05 ± 0.03 0.30 ± 0.05*** PAL × C -0.06 ± 0.26 -0.23 ± 0.08** PAL × F -0.11 ± 0.02*** -0.15 ± 0.04***
AICc 1505.06 2324.62 958.59 967.93 * P<0.05; ** P<0.01; ***P<0.001
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Figure 2. (a) Relationship between total abundance of flower visiting insects and PAL for organic and conventional field centres and margins; and (b) relationship between total abundance of flower visiting insects and PAL for organic cereal and legume field centres. The lines represent the marginal predictions of Model 1 in Table 1 (Figure 2a) and Table 2 (Figure 2b).
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Fruit set
Fruit set of Raphanus sativus in cereal fields was affected by PAL and
management, and position (Fig. 3a). All three models yield a similar fit of
the data (Table 3); the best fitting model was the one containing landscape,
management and position factors, although management by itself was not
statistically significant. PAL had a significantly negative effect on the fruit
set of the target plants. However, it interacts significantly with management,
implying that the differences between organic and conventional fields were
only important for “extreme” landscapes; either with a high or a low PAL.
Management and position also interacted significantly
(Table 3, M × P), whereas the fruit set of R. sativus was barely dissimilar
between margins and centres of conventional fields, there were stronger
differences in relation to position in organically managed fields. The models
including flower resources or insect abundances indicate that these variables
had a positive effect on fruit set. However, their interactions with PAL were
of opposite sign: whereas increasing PAL and flower resources had a
negative effect on fruit set, increasing PAL and insect abundances had a
positive effect on fruit set.
In organic field centres the differences between models were minimal
(Table 4, Fig. 3b). While most factors had the same sign as in cereal fields,
the abundance of flower resources was the only statistically significant
effect, favouring the fruit set of the target plants.
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Table 3. Effect of the percentage of arable land (PAL), management (organic vs. conventional) and position (margin vs. centre), corresponding to the Model 1; the effect of PAL and the abundance of flower resources, corresponding to the Model 2; and the effect of the abundance of flower visiting insects, corresponding to the Model 3, on the fruit set of Raphanus sativus in conventional and organic cereal fields. Green entries indicate statistically significant positive effects, red entries statistically significant negative effects and black entries are non-significant effects. On the last row, the Akaike Information Criterion for the best fitting model for each response variable is indicated in bold.
Model 1 Model 2 Model 3 PAL -0.46 ± 0.14*** -0.25 ± 0.12* -0.37 ± 0.11**
Management (M) -0.24 ± 0.17
Position (P) -0.08 ± 0.02**
Flower resources (F) ± 0.15 ± 0.02***
Apoidea ± -0.04 ± 0.02
Coleoptera ± 0.08 ± 0.03**
Diptera ± -0.05 ± 0.03
PAL × M 0.35 ± 0.17*
PAL × P -0.00 ± 0.02
M × P 0.50 ± 0.03***
PAL × F -0.13 ± 0.02***
PAL × Apoidea 0.25 ± 0.02***
PAL × Coleoptera 0.07 ± 0.02***
PAL × Diptera 0.07 ± 0.02***
AICc 6583.27 6744.36 6675.52 * P<0.05; ** P<0.01; ***P<0.001
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Table 4. Effect of the percentage of arable land (PAL) and crop type (cereal vs. legume), corresponding to the Model 1; the effect of PAL and the abundance of flower resources, corresponding to the Model 2; and the effect of the abundance of flower visiting insects, corresponding to the Model 3, on the fruit set of Raphanus sativus in organic field centres. Green entries indicate statistically significant positive effects and black entries are non-significant effects. On the last row, the Akaike Information Criterion for the best fitting model for each response variable is indicated in bold.
Model 1 Model 2 Model 3 PAL -0.21 ± 0.18 -0.06 ± 0.13 -0.24 ± 0.17
Crop (C) 0.20 ± 0.27
Flower resources (F) 0.34 ± 0.13**
Apoidea 0.02 ± 0.17
Coleoptera -0.01 ± 0.32
Diptera -0.11 ± 0.13
PAL × C 0.25 ± 0.26
PAL × F 0.15 ± 0.10
PAL × Apoidea 0.09 ± 0.16
PAL × Coleoptera 0.12 ± 0.23
PAL × Diptera 0.07 ± 0.12
AICc 3351.53 3347.05 3360.92 * P<0.05; ** P<0.01
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Figure 3. (a) Relationship between average fruit set and PAL for organic and conventional field centres and margins; and (b) relationship between average fruit set and PAL for organic cereal and legume field centres. The lines represent the marginal predictions of Model 1 in Table 3 (Figure 3a) and 4 (Figure 3b).
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The effects of landscape and field level variables on flower visitors
Landscape
Our results support that landscape level intensification affects negatively the
abundance of flower-visiting insects, in agreement with previous studies that
show that many flower visitor communities tend to be poorer in agricultural
landscapes with a lower presence of natural and seminatural habitats
(Bommarco et al., 2010; Westphal et al., 2008; Winfree, Aguilar, Vázquez,
LeBuhn, & Aizen, 2009). Non-agricultural habitats support many wild
flower visitors, which forage also on agricultural land (Billeter et al., 2008;
Holland, Smith, Storkey, Lutman, & Aebischer, 2015; Scheper et al., 2013).
However, we have found that these effects are not consistent among the
groups of flower visitors, and more importantly, our results diverge from
previous findings in important ways. Our results show that, in our study area,
the negative response of flower-visitors to PAL is mainly driven by Diptera,
whereas bees and flower-visiting Coleoptera are favoured by increasing
agricultural land-use around the fields. Some authors have suggested that the
amount of high-quality (non-agricultural) habitats can favour bees (Kennedy
et al., 2013). However, Westphal et al. (2003) indicated that it is required a
very low percentage of seminatural habitats to sustain the populations of
bumblebees. The contrasting response of the different groups of insects to
PAL suggests that other features of the landscape, such as crop diversity
(Hass et al., 2018) or even density of field margins (Dainese et al., 2017), can
have diverse effects on different groups with different requirements, and this
may help to explain why some organisms respond positively to increasing
agricultural land use in the landscape (Carré et al., 2009; Westphal et al.,
2003; Winqvist, Ahnström, & Bengtsson, 2012).
DISCUSSION
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Effect of field margins
The distance to field margins, on the other hand, has a more consistent
positive effect on the abundance of flower visitors. Margins have been
shown to concentrate the activity as well as the diversity of many groups of
invertebrates (Gabriel et al., 2010), and this pattern seems to be independent
of the quality of field margin habitats, at least locally (Dainese et al., 2017).
The overall abundance of flower visiting insects may be determined by
surrounding landscape, but our results demonstrate that cereal fields,
although visited, are not a favoured environment, and the activity density of
flower visiting insects is higher in field margins (although see below for the
joint effects of field margins and management). Cereal fields in general may
host few species that need to be insect-pollinated and thus the resources for
insects are scant (Gabriel & Tscharntke, 2007; José-María et al., 2011).
However, the role of margins goes far beyond the mere provision of feeding
resources, as they channel insect movement (Hass et al., 2018), which may
explain why flower visiting insects are more abundant in field edges even in
flower-rich crops such as oilseed rape (Stanley, Gunning, & Stout, 2013) and
to some extent it may also explain why it is more important the amount than
the quality of woody margins (Dainese et al., 2017).
Effect of crop management
Our results indicate that the effects of in-field characteristics, as determined
by management and crop, are less consistent, particularly because of its
interactions with position. Brittain et al. (2010) studied the effects of
management in a context where insecticides are routinely applied under
conventional farming, and found that organic farming did not have a positive
effect in isolated organic farms, thus pointing at the importance of
surroundings when considering the effects of within-field management. In
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general, however, it has been shown that richness of insects is reduced by
increasing management intensity (Hendrickx et al., 2007).
Our results support a positive effect of organic farming on the overall
abundance of flower visitors, but there are interactions between management
and the landscape or the position within the field, and these interactions
depend on the group of flower visitors. In general, however, the presence of
organic farming tends to smooth out the effects of both landscape and
position. Some authors have also found interactions between landscape and
organic management in the same direction (Batáry, Báldi, Kleijn, &
Tscharntke, 2011; Holzschuh, Steffan-Dewenter, Kleijn, & Tscharntke,
2007). Cereal fields have a very low foraging quality for flower-visiting
insects. Organic farming alleviates this deficiency, smoothing the effects of
landscape (by concentrating the activity of insects) or position (by having
more insect-appealing field centres). Nevertheless, the positive effects of
organic management are restricted to the cereal field centres (no differences
between margins and centres, and no differences compared to conventional
margins). This fact may indicate that either the positive effects of organic
farming for insects are very restricted in space, unlike plants which are
favoured also in field margins by organic farming (Bassa et al., 2012; José-
María et al., 2010), or that indeed the quality of field margins is irrelevant
(Dainese et al., 2017). One possible explanation of this behaviour relates to
concentration and dilution effects in conventional and organic fields,
respectively. In our study, overall flower visitor abundance seems to be
determined by the landscape structure; and most insects remain close to
favoured habitats, i.e. field margins. The interaction between management
and position implies that, in conventional cereal fields, flower visitors tend to
concentrate much more on field margins, whereas in organic fields the better
conditions of field centres cause a dilution of flower visitors, similar but
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weaker to that caused by mass flowering crops (Holzschuh et al., 2016,
2011).
The effects of flower resources
In Mediterranean cereal-devoted landscapes, where the application of
insecticides is low or inexistent (Caballero-López et al., 2011), the effects
attributable to PAL, management, and position within fields could be
attributed to flower resources on the one hand, and availability and
connectivity of nesting and alternative foraging habitats on the other hand.
Some studies indicate that organic fields with an equivalent level of flower
resources than conventional counterparts do not differ significantly from
them (Brittain et al., 2010). Our models including flower resources indicate
that they have a positive and significant effect for all groups, as well as for
the whole ensemble of flower visitors, and that it is largely independent of
landscape effects. However, only the model for total abundance of flower
visitors that comprises flower resources is better (lower AICc) than its
counterpart comprising all experimental factors. For bees, flower-visiting
flies and flower-visiting beetles the models including the experimental
factors are better than the ones containing flower resources. It is known that
flower resources exert a positive effect on the abundance of flower visitors,
but that they only determine a small fraction of insect distribution (Torné-
Noguera et al., 2014). Therefore, management and position have effects
beyond increased availability of flower resources, as it has been discussed
(see above; Dainese et al., 2017; Hass et al., 2018). Flower resources may be
of limited use for predicting flower-visitor abundance owing to their
transient nature, and thus the effects of long-lasting factors or landscape
structure may be more important (Torné-Noguera et al., 2014).
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Effect of legumes
Legumes differ from cereals in many characteristics, from vegetative tissue
quality to the offer of floral and extra-floral nectar (Caballero-López et al.,
2011), so their effect should be comparable to that of flower resources in
general. However, the role of legumes favouring flower visitors is even more
tenuous than that of flower resources. Our results do not support a significant
effect of legumes or their flower resources except for flower-visiting beetles.
Other authors have attributed the negative effects of non-cereal crops to their
management, which was considered more negative than that of cereals (Hass
et al., 2018). This is not our case, as the selected organic legume fields do not
receive any pesticides and their management is like that of organic cereals.
Although there is a slight increase of flower visitors’ abundance in these
fields, this effect is significant only for flower visiting beetles and mainly in
low-intensity landscapes. Beetles are the least mobile of the studied groups,
and may respond positively even to a non-preferred flower resource.
The effects on fruit set of the target species
One of the objectives of our research was to test how do the effects on the
community of flower visitors translate into the pollination of target plants.
Raphanus sativus flowers are prone to unspecialized interactions with a
broad array of flower visiting insects (Mendoza-García et al., 2018; Steffan-
Dewenter & Tscharntke, 1999). This feature should increase the chances of
detecting a response of fruit set irrespective of the group of insects involved
in the interaction with it.
One possible outcome would have been that the fruit set of target
plants was dependent on insects, which may depend on flower resources, and
in its turn dependent on landscape, position and management. However, only
for organic field centres seems that the abundance of flower resources is the
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best predictor of fruit set, and, in general, the experimental factors
(landscape, management, position) are a better predictor of fruit set. The
increased availability of flower resources in organic crops, crop margins and
in legume crops can enhance the delivery of pollination and thus fruit set of
the target plant. This effect is consistent when considering both cereal fields
and legumes. In legume fields, in fact, the fruit set of target plants becomes
independent of the landscape conditions. Contrary to other studies, we have
not found a competition for pollinators, which may explain the decrease in
the fruit set of target plants owing to the abundance of surrounding flower
resources under certain circumstances, particularly near the presence of
mass-flowering crops (Holzschuh et al., 2011; Mendoza-García et al., 2018).
Our results support the positive effect of surrounding floral abundance on the
facilitation of pollination services (Hardman et al., 2016; Morandin &
Winston, 2006).
Our experimental design allowed us to detect a negative effect of
increasing PAL on the fruit set of the target species, which is consistent with
the reduction in the overall abundance of flower visitors in response to
decreasing the extent of non-agricultural habitats in the landscape. This
agrees with our hypothesis and with previous studies (Albrecht et al., 2007;
Steffan-Dewenter & Tscharntke, 1999) but seems to contradict the
suggestions by other authors that plants may not suffer from pollinator
limitation as dominant pollinators persist under agricultural expansion
(Kleijn et al., 2015). Our results support that even for unspecialized
pollination plants the detrimental effects of agricultural intensification at
landscape level on flower visitors can impinge a decrease of pollination
delivery.
The relationship to the quality of the flower visitors’ assemblage can
only be hypothesized. In our case, the response of the target plants does not
relate to the abundance of bees. We have found that bees (Apoidea) correlate
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positively with increasing PAL, which is at odds with published studies that
claim a negative effect of intensification on bees and their pollination
services (Kremen et al., 2002). Species-specific effects may be responsible
for the disparity of results and interpretations in previous studies. Despite
these patterns related to specific groups, the effect on R. sativus fruit set was
as expected. This result reinforces the idea that it is important to consider the
ensemble of flower visiting insects for the delivery of pollination services,
and not a single focal group (Garibaldi et al., 2014; Rader et al., 2016).
However, the nexus between the explored factors is complex, and in fact our
results indicate that there is not a perfect match between insect abundance
and fruit set in target plants, as the best explaining model is the one
considering the experimental factors. Experimental factors summarize a
more complex set of conditions than it is possible to evaluate from point
measures of flower resources or flower visitor abundance, in the same way
that the organic-conventional dichotomy provides meaningful information
over individual practices (Puech et al., 2014), if actual visitation rates were
not obtained.
Organic management counteracts the negative effect of increasing
PAL, rendering fruit set of target plants largely independent of the landscape
conditions, whereas plants placed in conventional fields undergo a strong
(three times) reduction in fruit set from the lowest to the highest PAL. This
agrees with the several studies that claim, for diverse components of
agroecosystems from plant species richness to insect diversity and
abundance, that organic farming compensates the negative effects of the
landscape (José-María et al., 2010; Rundlöf & Smith, 2006; Tscharntke et
al., 2005).
Less clear is the effect of position within fields, as the effect of
position itself is low although significant, and there is a strong interaction
with management. The very high variability of fruit set dictates some
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prudency in this issue. Fruit set of target plants does not parallel the relative
total abundances of flower visitors, neither for conventional cereal, organic
cereal or organic legume fields. Only in organic cereal fields we found the
expected response of higher fruit set in field margins than in field centres, as
it matches the findings on pollen transfer along field margins by other studies
(Hass et al., 2018). These results indicate a decoupling of flower visitors and
actual pollination rates. Insect abundance, even if filtered to keep only the
more flower dependent groups, may conceal the actual value of insect
community for pollination (Grass, Bohle, Tscharntke, & Westphal, 2018).
However, most importantly, fruit set does not parallel the abundance
of bees or any other individual group. Our phytometer species, being not
very selective in its interaction with flower visitors, may not suffer seriously
from the decline of any particular group, but it indicates how changes in a
generalist-dominated interacting community can affect overall levels of
pollination (Grass et al., 2018; Potts et al., 2010).
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It has been proposed that ecosystem-service-based arguments are an
insufficient reason to preserve the biological diversity of pollinators (Kleijn
et al., 2015). But there are strong indicia that tell us that declining flower-
visiting insect abundance can indeed affect pollination services (Potts et al.,
2010; Vanbergen et al., 2013) and that this decline can have strong effects on
the global economy (Gallai et al., 2009). It is necessary to implement
efficient measures that stop the decline of flower-visiting insects, and that
promote the delivery of pollination services. However, favouring flower-
visitors and plant pollination may require different approaches, particularly
because a “one for all” solution may be ineffective. On the one hand, the
preeminent concern about bees may hinder the recognition that many insects
apart from bees may be involved in pollination networks and deliver
effectively the pollination service (Rader et al., 2009, 2016); on the other
hand, it does not consider that there may be an enormous variation in specific
insect responses (Grass et al., 2016). But more importantly, that the interplay
between flower visitors and plant pollination and fruit set is a complex
process, in which the result is not fully determined by each of the
components, at the landscape or the field level (Grass et al., 2018). Despite
these limitations, our results make us to conclude that preventing landscape
simplification, deploying organic agriculture, preserving field margins and
increasing flower resources at the field level may increase the presence of a
diverse community flower visitors in agricultural landscapes, which in turn
can help to maintain or increase fruit set levels under many circumstances.
Acknowledgements We are very grateful to the farmers who allowed us to use their fields, and students for their collaboration in processing the insect and plant samples. We also thank J. Mederos and A. Viñolas for their help identifying insects. This research was funded by the project “Agricultural intensification, biodiversity and pollination functioning in the Mediterranean region. Development of environmentally friendly farming schemes” and a FPI-MEC grant to MMG from the Spanish Government.
CONCLUSIONS
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Albrecht, M., Duelli, P., Müller, C., Kleijn, D., & Schmid, B. (2007). The Swiss
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Figu
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SUPPLEMENTARY MATERIAL
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Table S1. Total abundance of flower-visiting insects captured over the six sampling periods in each of the fields, split by position (field centre – C – or field margin – M –). The symbol “-“ denotes an experimental combination that was not sampled.
Apoidea Diptera Coleoptera Locality code Management Crop C M C M C M
Su su conventional cereal 15 18 143 191 24 66
organic cereal 18 15 76 102 42 85
organic legume 21 - 117 - 32 -
Cardona car conventional cereal 6 15 125 187 34 32
organic cereal 10 11 261 213 15 75
Montmajor mon conventional cereal 12 19 131 168 91 242
organic cereal 4 6 80 81 52 94
organic legume 13 - 86 - 76 -
L’Espunyola esp conventional cereal 3 9 173 249 36 55
organic cereal 6 35 152 150 65 139
organic legume 9 - 381 - 77 -
Balsareny bal conventional cereal 3 5 84 94 29 103
organic cereal 4 2 37 50 40 184
organic legume 2 - 146 - 53 -
Santa Maria d’Oló
olo conventional cereal 10 6 214 173 77 79
organic cereal 19 12 272 220 39 175
organic legume 22 - 617 - 85 -
Moià (B) mob conventional cereal 3 14 176 96 50 184
organic cereal 6 7 589 96 47 180
organic legume 4 - 173 - 135 -
Castellterçol cas conventional cereal 1 2 301 311 65 73
organic cereal 4 2 175 50 54 48
Moià (A) moa conventional cereal 2 14 181 441 47 90
organic cereal 2 20 215 530 24 23
organic legume 2 - 584 - 64 -
Vic vic conventional cereal 2 8 509 198 175 423
organic cereal 6 7 655 238 256 436
organic legume 13 - 244 - 286 -
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Table S2: List of the species (according to de Bolòs et al. 2005) that accumulated at least the 90% of the flower resources surveyed in all transects. The figures in the table are average flower abundances for the whole sampling period and the whole set of localities. The symbol “-“ denotes the absence of a species under a given experimental condition. The * symbol after an average abundance indicates a species that constitutes the crop in at least one of the fields surveyed. On the last two rows, the global average flower resource abundance and total number of species identified in each of the experimental conditions is indicated.
Conventional cereal
Organic cereal
Organic legume
centre margin centre margin centre Anthemis cotula L. - - 10 110 117
Arenaria serpyllifolia L. - 94 - 20 -
Ballota nigra L. - 98 - 2850 285
Campanula rapunculoides L. - 70 - - -
Capsella bursa-pastoris (L.) Medik. 19 19 574 246 71
Carduus tenuiflorus Curtis - 15 - 238 21
Caucalis platycarpos L. - 513 - 7 19
Cirsium arvense (L.) Scop. 188 16 - 192 20
Convolvulus arvensis L. 113 28 9 28 8
Diplotaxis erucoides (L.) DC. - 54 109 100 39
Echium vulgare L. - 110 - 586 356
Erodium cicutarium (L.) L'Hér. ex Aiton
- 133 - 15 -
Erucastrum nasturtiifolium (Poir.) O.E. Schulz
- 180 40 11 -
Fumaria officinalis L. 105 109 67 259 353
Galium lucidum All. - 1748 - 2600 -
Galium tricornutum Dandy - 42 55 7 33
Genista scorpius (L.) D.C. - 5508 - - -
Lepidium draba (L.) Desv. - 146 - - -
Malva sylvestris L. - 116 9 434 949
Marrubium vulgare L. - - - 262 36
Matricaria maritima subsp. inodora L.
- - 11 445 -
Medicago lupulina L. - 68 - 11 -
Medicago minima L. - 12 - 111 -
Medicago polymorpha L. 3 85 286 73 51
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Medicago sativa L. - 374 166 348 306
Odontites vernus (Bellardi) Dumort. - - - 116 -
Onobrychis viciifolia Scop. - - - 236 14156*
Papaver rhoeas L. 16 105 181 115 405
Pisum sativum L. - - - - 2156*
Ranunculus bulbosus L. - 158 - 36 -
Raphanus raphanistrum L. - - 58 242 -
Rapistrum rugosum (L.) All. - - 297 226 1102
Reseda phyteuma L. - - 75 - 9
Robinia pseudoacacia L. - - - 112 -
Rubus canescens D.C. - - - 197 -
Scandix pecten-veneris L. - 540 21 655 1
Sideritis hirsute L. - - - 251 -
Sinapis alba L. - - - - 428*
Stellaria media (L.) Vill. 50 34 118 404 117
Torilis arvensis (Huds.) Link - 611 - 1729 1256
Trifolium campestre Schreb. in Sturm
- 332 - 39 -
Veronica arvensis L. 17 21 - 9 36
Veronica hederifolia L. 6 119 21 23 32
Veronica persica Poir. in Lam. 24 53 45 50 55
Veronica polita Fr. 21 13 - - 1
Vicia cracca L. - 1 924 688 268
Vicia ervilia (L.) Willd. - - - - 593*
Vicia sativa L. 16 14 267 72 57
Vicia villosa Roth. - - - 112 -
Viola arvensis Murray 25 41 8 8 157
Global average 40.1 152.0 97.7 183.8 453.9
Total number of species 16 82 36 83 54
CAPÍTULO 2
Farming practices and flower resources determine plant reproduction in Mediterranean landscapes Marian Mendoza-García, Péter Batáry, José M. Blanco-Moreno, Lourdes Chamorro, F. Xavier Sans En fase de preparación para su envío a Biological Conservation
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Organic farming practices are thought to mitigate pollinator decline in
intensive agricultural landscapes and, in consequence, could improve
pollination services. However, there is scarce information on the effect of the
proportion of organically managed arable land (POL) and local flower
resources (local flower cover and local land use and management) on
pollinator abundance and pollination. We evaluated pollinator abundance and
pollination delivery in five landscapes varying in their proportion of
organically managed arable land. We placed pan traps and two phytometer
species with different pollination syndromes in field margins of both organic
and conventional cereal fields and legume fields. Bee abundance was not
enhanced either by POL at landscape scale or by local flower cover. Bee
abundance did not also increase in field margins next to legume crops,
probably caused by abundant food resources that lead to pollinator
dilution. POL enhanced the fruit set of the generalist species, whereas it did
not influence the specialist species. The increase in local flower cover in
field margins negatively affected the fruit set, because competition for
pollinators could occur between the phytometer species and species thriving
in plant communities. Despite the negative effect of local flower cover, the
fruit set benefited from nearby legume crops. In conclusion, policies
ameliorating landscape features (e.g. increasing flower abundance) coupled
with the promotion of organic farming at the regional level and insect-
pollinated and flower-rich crops (e.g. legumes) are the main ways to improve
pollination services in Mediterranean arable landscapes, even if they have
poor effects on bees.
Keywords
Agri-environment schemes, bees, ecosystem services, flowering plants,
organic farming, pollination syndromes, spatial scales
SUMMARY
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Biodiversity decline is mainly caused by the intensification of agriculture, in
both natural areas and agroecosystems (Tscharntke et al., 2012).
Consequently, ecosystem services, such as pollination and pest control, are
negatively affected. One of the main aims of agri-environment schemes
(AES) is the protection and conservation of biodiversity and ecosystem
services in agricultural landscapes (Batáry et al., 2015). Environmentally
friendly agricultural practices are implemented to mitigate biodiversity loss.
In particular, organic farming is characterized by long crop rotations and by
limiting the use of synthetic fertilizers and pesticides (Reganold and
Wachter, 2016; Seufert and Ramankutty, 2017). This practice often benefits
the abundance and diversity of pollinators (Holzschuh, Steffan-Dewenter, &
Tscharntke, 2008; Rundlöf, Nilsson, & Smith, 2008a), which in turn can
potentiate pollination services (Gabriel and Tscharntke, 2007).
Several studies have demonstrated that the benefits of AES and
organic farming depend on landscape heterogeneity (Batáry et al., 2011;
Rundlöf and Smith, 2006; Tuck et al., 2014). Plant and pollinator diversity
can be affected by the proportion of organic farming in the landscape and the
extension and quality of non-cropped habitats (Power et al., 2012). In
addition, the effects of organic farming can vary among groups of organisms
and spatial scales (Batáry et al., 2011; Bengtsson et al., 2005; Fuller et al.,
2005; Rundlöf and Smith, 2006). Thus, the understanding of biodiversity
patterns in agricultural landscapes requires the study of multiple scales
(Concepción et al., 2008; Tscharntke et al., 2005).
In many agricultural landscapes, organic fields are embedded in a
matrix of conventional fields, regularly combined with a low heterogeneity
in the surrounding habitat (Fuller et al., 2005). For instance, Rundlöf and
Smith (2006) showed that butterfly species richness and abundance were
positively affected by organic farming in homogeneous intensively managed
INTRODUCTION
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landscapes. Similarly, bee diversity was enhanced by organic farming more
in homogeneous landscapes than in heterogeneous landscapes (Holzschuh et
al., 2007). In a meta-analysis, Batáry et al. (2011) found that agri-
environmental measures enhanced the abundance and species richness of the
principal groups of pollinators, but their response was determined by
landscape context. Agri-environmental schemes often benefits for example
crop pollination, more in simple than in complex landscapes, which can be
attributed to a spillover from surrounding habitats into the cropland (Kleijn et
al., 2011).
Insect-flower interaction networks differ in magnitude and
composition depending on the farming system (Power and Stout, 2011).
Organically managed fields support higher levels of plant abundance, species
richness, and diversity than fields with conventional farming, which in turn
can attract more pollinator visits (Chamorro et al., 2016). In consequence, the
increase in pollinator abundance can result in a higher visitation rate per
insect-pollinated plant (Power and Stout, 2011). Plant-pollinator interactions
are complex because they can be affected by a variety of factors. The
surrounding plant communities can increase the frequency of pollinator visits
via facilitation (Moeller, 2004; Waser and Real, 1979), or decreasing it via
competition (Marja et al., 2018; Pleasants, 1981). In addition, changes in
landscape composition can cause a dilution or concentration of pollinators,
which can alter plant-pollinator interactions (Tscharntke et al., 2012).
Most research focuses on the study of pollination through pollinators
or insect-plant interactions to evaluate the effect of organic farming.
However, the direct evaluation of fruit set could be a much better approach
to analysing the effect of organic farming on pollination services (Woodcock
et al., 2014). For instance, in a study that evaluated different wildlife-friendly
schemes, the fruit set of an open-flower plant pollinated by a broad group of
pollinators was higher in organic than in non-organic farming schemes
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(Hardman et al., 2016). Also, the fruit set of a self-incompatible plant
pollinated by a wide range of pollinators was higher in organic than in
conventional fields (Power and Stout, 2011). In contrast, a study of vineyards
found that pollination, measured as the fruit set and seed weight of an open-
flower plant, was negatively affected by the proportion of uncultivated land
in the surrounding landscape independently of the farming system (Brittain
et al., 2010). However, information about the impacts of organic farming and
local flower resources on the fruit set of both generalist and specialist plants
species remains scarce. By comparing a generalist with a specialist plant
species, it is possible to evaluate effects of farming practices on fruit set of
these two syndromes.
In this study, we evaluated the effect of the proportion of organically
managed arable land (POL) and local flower resources on the abundance of
bees (Hymenoptera: Apoidea) and on the fruit set of two phytometer species
with different pollination syndromes (generalist vs. specialist) in organic and
conventional cereal and legume fields in Mediterranean agricultural
landscapes. Our mains questions are: (i) does POL and local flower resources
affect the bee abundance and fruit set of generalist and specialist plant? and
(ii) are there a difference in the effect on fruit set between the generalist and
specialist plant species? We expected that pollinator abundance could be
enhanced by the proportion of organically managed land and local flower
resources, which would thus increase the fruit set of phytometers. However,
we also expected a competition for pollinators between the local flower
resources and the phytometer species, which would result in a decreased fruit
set, that may be stronger in specialist insect visited plants (Fig. 1).
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Figure 1. General model to predict the effect of the organic farming system on pollination. Organic farming at the landscape scale can affect the pollination of plants through an increase in pollinator abundance (a: Holzschuh, Steffan-Dewenter, & Tscharntke, 2008; c: Power & Stout, 2011). Pollination also can be affected directly by the local flower resources, through competition for pollinators (d: Mendoza-García et al., 2018), or indirectly by changes in pollinator abundance (b: Ebeling et al., 2008; Grass et al., 2016). Black and red lines represent positive and negative effects, respectively.
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Study design
The study was conducted in 2015 in central Catalonia, northeast Spain (41°
32′-42° 3′ N 1° 35′-2° 14′ E; see Appendix S1 in Supporting Information).
The area is devoted mainly to the cropping of dryland cereals. Within the
region, five landscapes were selected to encompass gradients from low to
high proportion of organically managed arable land (POL). The five selected
landscapes were separated by at least 20 km. Within each study landscape,
we selected two organic and two conventional cereal fields and two legume
fields. The selected legume fields were under conventional or organic
management. The organic fields studied were managed according to the
European regulations on organic farming, characterized by the prohibition of
the use of any pesticides and synthetic fertilizers. In landscapes with the
lowest proportion of organic farming, we could not find two legume fields.
Proportion of organically managed arable land
We calculated the total arable land surface (excluding vegetable crops, fruit
cultivation, and any other crop) under organic management within a 500 m
radius for each individual field (Table S1). We used the relationship between
the proportion of organically managed fields and the arable land proportion
(proportion of organic agricultural land/proportion of arable land: mean ±
SD = 0.32 ± 0.25; range: 0.002-0.796) as an indicator of organically
managed arable land at the landscape scale. All GIS operations were
conducted on ArcGIS 10.2.2 (ESRI, 2010).
Local flower resources
We characterized the local flower resources by means of the local flower
cover and the local land use and management, which represent the resources
in the margin and edge, and in-crop, respectively. Both variables describe
MATERIALS AND METHODS
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different scales of flower resources in the field. To assess the local flower
cover, we surveyed the richness and abundance of flowering plants in
conventional and organic cereal and legume fields between May and June
2015. The surveys were conducted once a week for a duration of five weeks,
in two parallel transects of 1 × 16 m, in the studied fields. These transects
corresponded to the crop edge (first metre of the crop) and the field margin.
The abundance of flower resources was assessed by visual estimation of the
relative cover of flowers (expressed as a percentage). The local flower cover
was calculated as the mean of all species flower covers over the five surveys.
The local land use and management was described through the
different levels of crop attractiveness to pollinators (see Statistical Analysis
section). On one end of the spectrum, conventional cereal fields were
selected by their low weed abundance and species richness (Bassa et al.,
2011; José-María et al., 2010). On the other end, we sampled legume fields,
which, at least temporarily, can supply a significant amount of flower
resources, in addition to weed communities. Organic cereal fields were
characterized by an intermediate level of flower resources, which usually
host complex weed communities in terms of weed abundance and species
richness. Thus, conventional cereal fields, organic cereal fields, and legume
fields represented, in that order, a gradient of increasing crop attractiveness
to pollinators.
Bee surveys
We surveyed bee abundance using pan traps, which consisted of three cups
(500 mL, 160 mm diameter, Pro’Jet, Paris, France) painted with blue, yellow
and white UV reflecting spray colour (Sparvar Leuchtfarbe, Spray-Color
GmbH, Merzenich, Germany). One pan trap was placed in the margin of
each studied field. It was located 1 m above the ground and 1 m apart from
each group of phytometer species. Pan traps were filled with water and a
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small drop of detergent to reduce surface tension, and were operating for 12
h. The surveys were performed under favourable weather conditions (no rain,
low wind speeds, and diurnal temperatures above 18 °C), and were
conducted once a week for a duration of five weeks (between May and June
2015). Samples were stored in 70% alcohol, and specimens of Hymenoptera
were identified to family level. For this study, we only used data on bee
abundance (Hymenoptera: Apoidea).
Phytometer species and fruit set
We selected Raphanus sativus (Brassicaceae) and Onobrychis viciifolia
(Leguminosae) as phytometer species to evaluate the fruit set. R. sativus is an
annual plant that produces numerous symmetrical actinomorphic white
flowers on a broad-branched inflorescence. It is self-incompatible (Young
and Stanton, 1990) and commonly visited by a wide array of pollinators,
such as honey bees, bumblebees, wild bees, hoverflies and butterflies
(Albrecht et al., 2007; Steffan-Dewenter and Tscharntke, 1999). The
perennial O. viciifolia produces numerous zygomorphic melliferous pink
flowers on several unbranched inflorescences. It is an outbreeding insect-
pollinated species, almost entirely pollinated by bumblebees, honey bees,
and wild bees (Hayot Carbonero et al., 2011). Onobrychis viciifolia is an
obligate insect-pollinated species (Hanley et al., 2008). The difference in the
breadth of pollinator assemblage between both plant species allows the
classification of R. sativus as a generalist insect-pollinated species and O.
viciifolia as a specialist insect-pollinated species.
On January 2015, seeds of R. sativus and O. viciifolia were sown in
multipots. In the seedling stage, the plants were separated into 5 L pots filled
with commercial garden soil (a mixture of peat, vermiculite, and clay) and
were kept outdoors at the Experimental Field Service of the University of
Barcelona. Eight individuals of each phytometer species were transported to
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each field margin before the beginning of their flowering season. The plants
were grouped by species and were separated by 2 m. Every three to five
days, plants were watered, and the frequency was determined by the weather
conditions. After five weeks, the phytometer species were transported back
to a greenhouse at the Experimental Field Service to prevent any further
interaction with pollinators. Flower buds were removed to avoid the
overestimation of unpollinated flowers. We counted the number of well-
developed fruits and the number of flowers that were not pollinated (no
development of fruits). The fruit set was calculated as the proportion of
flowers that set fruit.
Statistical analyses
We tested the effects of the proportion of organically managed land (POL),
local flower cover (%), local land use and management (conventional and
organic cereal fields and legume fields), and bee abundance on the fruit set
of both phytometer species using structural equation modelling (SEM). This
method allows the evaluation of the indirect pathways that can influence the
fruit set of generalist and specialist insect-pollinated plant species, R. sativus
and O. viciifolia, respectively.
To include local land use (categorical variable) in the SEM, we
encoded it as a continuous variable, which represented a level of
attractiveness to bees. We considered that conventional cereal fields offered
the lowest amount of flower resources, whereas organic cereal fields and
especially legume fields represented an increased attractiveness, owing to
their higher abundance of flowers. We tested the effects of local land use
(cereal or legume) and management (organic or conventional) on the local
flower cover, to support our a priori categorization. Thus, we considered
local land use and management as an ordered factor variable with three
levels: conventional cereal, organic cereal, and legume (the latter
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independent of management type). We tested the differences in local flower
cover between the levels of this ordered factor through polynomial contrasts,
including a linear and a quadratic term. The model was analysed with a
linear mixed-effects model with normal error distribution, using the
landscapes as a random effect factor. We also evaluated the effects of local
land use and management on the fruit set of both phytometers.
The initial SEMs (Figs S1 and S2) contained all possible paths,
including the correlations between the POL and the variables describing the
local flower resources (direct survey of the local flower cover and local land
use and management). To simplify the initial SEM and obtain the minimal
SEM, a backward selection was conducted. We used the Akaike information
criterion (AIC) to select the best model (Shipley, 2013).
SEMs included the following models: (i) the bee abundance was
analysed with a linear mixed-effects model with normal error distribution,
and (ii) the fruit set of the phytometer species was analysed with a
generalized linear mixed-effects model with binomial error distribution. The
bee abundance data were log-transformed to meet the assumptions of
normality and homoscedasticity of residuals. We performed separate SEMs
for the two phytometer species. In all models, we used the landscape identity
(five levels) as a random effect factor to control for within-landscape
correlation. The proportional contributions of direct and indirect pathways on
the fruit set of both phytometer species were calculated using the
standardised path coefficients (based on Grace and Bollen, 2005). The
statistical analyses were conducted using the packages piecewiseSEM
(Lefcheck, 2016) and lme4 (Bates et al., 2015) on R software version 3.3.2
(R Development Core Team, 2016).
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Local land use and management
We found a strong linear effect of local land use and management
(conventional and organic cereal fields and legume fields) on the local flower
cover (Table S2; Fig. 2a). The difference in local flower cover was about the
same magnitude between conventional cereals and organic cereals as than
between organic cereals and legumes. Additionally, the fruit set of both
phytometer species were higher in plants located next to legume fields than
those next to organic and conventional cereals fields (Table S2; Figs 2b-c).
Structural Equation Modelling
The fruit set of the generalist insect-pollinated plant species, R. sativus, was
enhanced by bee abundance. However, local flower cover negatively affected
the fruit set, even when its effect on the abundance of bees was non-
significant. The effect of the POL was also non-significant on bee
abundance, but it had a positive effect on the fruit set. In addition, the local
land use and management enhanced the fruit set of R. sativus (Fig. 3a and
Fig. S1). The proportional contribution of the POL to the estimated total
effect on the fruit set of R. sativus was 16.7%. Local flower cover negatively
affected the fruit set by 31.7%. Local land use and management and bee
abundance contributed 20.2% and 31.5% to the fruit set, respectively
(Fig. 3b).
The fruit set of the specialist plant species, O. viciifolia, was not
enhanced by the increase in bee abundance, in contrast to the findings for R.
sativus. Nevertheless, like the generalist plant species, the fruit set of O.
viciifolia was decreased by local flower resources and enhanced by the local
land use and management. The fruit set of O. viciifolia had a lower
dependence on landscape identity than did the abundance of bees and the
fruit set of R. sativus. The proportion of organically managed land, neither
RESULTS
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indirectly through the bee abundance, nor directly, affected the fruit set of
the specialist phytometer species (Fig. 4a and Fig. S2). The local flower
cover negatively affected the fruit set of O. viciifolia by 61.1%, whereas the
local use and management contributed by 38.9% (Fig. 4b).
Figure 2. (a) Mean (± SE) of (a) local flower cover, (b) fruit set of Raphanus sativus and (c) fruit set of Onobrychis viciifolia in relation to the local land use and management (conventional cereal fields, organic cereal fields, and legume fields).
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(a)
(b)
Figu
re 3
. (a)
Fin
al S
EM
mod
el f
or th
e fr
uit s
et o
f Ra
phan
us sa
tivus
(Fi
sher
’s C
sta
tistic
: C =
0.5
9, p
= 0
.744
). U
nsta
ndar
dise
d pa
th
coef
fici
ents
are
sho
wn
for
the
bino
mia
l fru
it se
t m
odel
, sta
ndar
dize
d pa
th c
oeff
icie
nts
for
the
bee
abun
danc
e m
odel
, and
Pea
rson
’s
r co
rrel
atio
n co
effi
cien
ts f
or t
he c
orre
latio
n be
twee
n lo
cal
vari
able
s (l
ocal
flo
wer
cov
er a
nd l
ocal
lan
d us
e an
d m
anag
emen
t).
Mar
gina
l and
con
ditio
nal R
2 val
ues
are
show
n fo
r ea
ch r
espo
nse
vari
able
. Dot
ted
lines
rep
rese
nt n
on-s
igni
fica
nt e
ffec
ts. T
he w
idth
of
eac
h ar
row
is
prop
ortio
nal
to t
he p
ath
coef
fici
ents
. (b)
The
pro
port
iona
l co
ntri
butio
n of
sig
nifi
cant
ind
irec
t an
d di
rect
pat
hway
s to
the
est
imat
ed t
otal
eff
ect
of t
he P
OL
, loc
al f
low
er c
over
, loc
al l
and
use
and
man
agem
ent,
and
bee
abun
danc
e on
the
fru
it se
t of
R.
sat
ivus
, us
ing
the
stan
dard
ized
pat
h co
effi
cien
ts (
follo
win
g G
race
& B
olle
n, 2
005)
. P
OL
= p
ropo
rtio
n of
org
anic
ally
man
aged
ar
able
land
.
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(a)
(b)
Fi
gure
4. (
a) F
inal
SE
M m
odel
for
the
fru
it s
et o
f O
nobr
ychi
s vi
ciifo
lia (F
ishe
r’s
C s
tatis
tic:
C =
2.4
1, p
= 0
.66)
. U
nsta
ndar
dise
d pa
th c
oeff
icie
nts
are
show
n fo
r th
e bi
nom
ial
frui
t se
t m
odel
, st
anda
rdis
ed p
ath
coef
fici
ents
for
the
bee
abu
ndan
ce m
odel
, an
d P
ears
on’s
r c
orre
latio
n co
effi
cien
ts f
or t
he c
orre
lati
on b
etw
een
loca
l va
riab
les
(loc
al f
low
er c
over
and
loc
al l
and
use
and
man
agem
ent)
. M
argi
nal
and
cond
ition
al R
2 val
ues
are
show
n fo
r ea
ch r
espo
nse
vari
able
. D
otte
d lin
es r
epre
sent
non
-sig
nifi
cant
ef
fect
s. T
he w
idth
of
each
arr
ow i
s pr
opor
tiona
l to
the
pat
h co
effi
cien
ts.
(b)
The
pro
port
iona
l co
ntri
butio
n of
sig
nifi
cant
ind
irec
t an
d di
rect
pat
hway
s to
the
esti
mat
ed to
tal e
ffec
t of
the
PO
L, l
ocal
flo
wer
cov
er, l
ocal
land
use
and
man
agem
ent,
and
bee
abun
danc
e on
the
fru
it se
t of
O. v
iciif
olia
, us
ing
the
stan
dard
ised
pat
h co
effi
cien
ts (
follo
win
g G
race
& B
olle
n, 2
005)
. P
OL
= p
ropo
rtio
n of
or
gani
call
y m
anag
ed a
rabl
e la
nd.
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We evaluated the effect of local flower cover and POL on the abundance of
bees and the fruit set of generalist and specialist plant species. We have
shown that it is possible to modify the fruit set of target species by the
variation in local availability of flower resources at different spatial scales,
but that the effects are in opposite directions at these lower levels of action;
an increased field level resource availability can enhance the delivery of
pollination services, whereas increased resources at a very local level
(neighbouring to target plants) may actually decrease the fruit set. In
addition, our study provides the first evidence that the fruit set of plants that
vary in pollination syndrome respond differently to the POL. Only the fruit
set of the generalist plant species was enhanced by the POL.
Bee abundance
The effects of organic farming on biodiversity are reported to be
heterogeneous (Clough et al., 2005; Ekroos et al., 2008; Purtauf et al., 2005;
Tuck et al., 2014). Our findings showed that the bee abundance was not
enhanced by the POL at the landscape scale, which is in accord with other
studies on bees (Brittain et al., 2010; Happe et al., 2018). Particularly, bees
depend on different habitat types for their nesting and foraging requirements,
which do not coincide often (Westrich, 1996). In fact, bee abundance can be
supported by nearby natural habitat more than by organic farming (Winfree
et al., 2008). For instance, bumblebees were not promoted by organic
farming, but they benefited from landscapes dominated by small size fields,
where the abundance of field margins between crops was higher (Happe et
al., 2018). We therefore suggest that bee abundance could depend more on
the surrounding habitat heterogeneity in the landscape than on the POL,
which by itself may not provide the necessary conditions for bee
enhancement.
DISCUSSION
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In contrast to our results, Holzschuh et al. (2008) showed that an
increase in the proportion of organic crops in the landscape enhanced species
richness and density of bees. Their findings were in part attributed to
differences in the flower cover, both in the field margins and in the crop, and
to the absence of insecticide application in organic compared to conventional
fields. In addition, when organic fields are embedded in a matrix of
conventional fields, it is possible that they did not offer enough resources to
enhance bee abundance (Rundlöf, Bengtsson, & Smith, 2008b). In this sense,
bees could concentrate their activity density only in the patches which
provide the highest amount of resources.
Contrary to our expectations, flower resources located at field
margins did not enhance bee abundance, independent of the farming system
of the adjacent field. In their study, Brittain et al. (2010) showed that flower
resources situated between fields were cut down, both in organic and
conventional fields. As a consequence, pollinators did not obtain enough
benefits from field margins. Similarly, Winfree et al. (2008) did not find any
effect of organic farming on flower visitation by bees. The authors suggested
that the main cause of this was the low variation in flower diversity between
farming systems. Thus, measures focusing on the promotion of flower strips
may not suffice to enhance bee abundance.
The availability of resources in the landscape can be supported not
only by field margins and edges, but also by crops providing flower
resources, such as legumes. Some studies have found that pollinator visits
can increase with the availability of resources offered by crops, especially
during their blossoming period (Ebeling et al., 2008). We expected an
increase in bee abundance in the field margins promoted by legume crops,
but we did not observe any effect on their abundance. These results can be
explained through the pollinator dilution caused by abundant food resources,
such as those from legume crops in bloom (Veddeler et al., 2006). For
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instance, the expansion of mass-flowering crops caused a dilution effect on
pollinators (Holzschuh et al., 2016). Therefore, our results seem to suggest
that the abundance of bees can be affected differently by flower resources
offered in the immediate vicinity and at the field level.
Fruit set
Most studies have focused on species with an open floral structure, which are
visited by a wide array of pollinators (Brittain et al., 2010; Hardman et al.,
2016; Power and Stout, 2011). Even though these studies focused on a fairly
homogeneous set of phytometer species, mixed results have been found
about the effects of organic farming on their pollination. In line with our
results for the generalist plant species, Power and Stout (2011) and Hardman
et al. (2016) showed that organic farming had positive effects on pollination
services, promoted by the high cover of flower resources and pollinator
abundance. In contrast, Brittain et al. (2010) found no difference in
pollination services between organic and conventional fields, which was
related to low differences in the abundance of pollinators between farming
systems. Likewise, we did not find differences in the abundance of bees,
which are the main flower visitors of the specialist plant species.
The enhancement of fruit set of the generalist phytometer species by
POL could be mediated not only through the bee abundance, but also by the
activity of other flower visitors. The POL had a positive effect on the fruit set
of the generalist species, which nevertheless requires the implication of
flower visitors. Considering that bee abundance was not affected by the POL,
plant pollination might be mediated by non-bee flower visitors. Although
these non-bee flower visitors have lower pollen loads, their rate of visit can
compensate for their low pollen deposition contribution when compared to
bees (Rader et al., 2016). Consequently, other non-bee flower visitors could
also support pollination services in agricultural landscapes. Flower resources
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can also benefit some non-bee flower visitors in the landscape (Grass et al.,
2016). For instance, organic farming in grassland systems enhanced the
abundance of hoverflies compared to conventional management (Power et
al., 2016). On the other hand, the fruit set of the specialist phytometer species
seems to depend more on local flower resources than on the organic
management of neighbouring fields or the abundance of bees.
Despite the contrasted pattern found in the fruit set of the phytometer
species in relation to POL, the effect of local flower cover was similar on
both plant species. The increase in the local flower cover in the field margins
and edges negatively affected the fruit set. In addition to pollinators, the
surrounding plant community can also affect pollination services (Kremen et
al., 2007). Competition for pollinators could occur between the phytometer
species and the species thriving in plant communities in the immediate
vicinity (Mendoza-García et al., 2018; Pleasants, 1981). In communities
where competition occurs among numerous plants, the movement of pollen
between flowers of different plant species by pollinators (interspecific pollen
transfer) can reduce the effectiveness of pollination (see Morales and
Traveset, 2008). Our findings showed that the local land use and
management had a positive effect on the fruit set of both phytometer species,
and this effect was higher in the specialist plant species. Facilitation between
plant species can occur when the floral forms are similar (Ghazoul, 2006), as
they may benefit from the concentration of a common set of effective
pollinators. We suggest that the flower similitude between legume crops and
the specialist plant species, which also belongs to the family Leguminosae,
improved the fruit set of the latter, compared to that of the generalist plant
species. In conclusion, the temporal availability of flower resources, for
instance offered by legume fields included in the crop rotation, can affect the
fruit set of the phytometer species.
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Our results provide evidence that local flower resources and the proportion
of organically managed arable land affect the fruit set of plants. Conversely,
bee abundance does not depend on farming practices. Instead, other flower
visitors could benefit from these landscape conditions and can deliver
effective pollination services. Agri-environmental schemes should promote
heterogeneous landscapes through the conservation or creation of landscape
features, for instance field margins, as well as avoid the use of agro-
chemicals (Pe’er et al., 2017) to promote the abundance of bees and other
flower visitors. Our study also demonstrated that legume crops in dryland
cereal cropping regions can improve the fruit set, particularly the one of
specialist plant species. In concordance with the greening measures of the
European Common Agricultural Policy, we recommend the inclusion of
legume crops, which, apart from delivering other agronomic services, can
also offer temporally abundant flower resources. We conclude that agri-
environmental policies should incorporate landscape and local management
options to support pollinator abundance and plant reproduction, which
include not only a higher proportion of organic farming in the landscape, but
also crops that are rich in flower resources.
Acknowledgements
We are very grateful to the farmers who allowed us to use their fields, and A. Pérez, R. Rotchés-Ribalta and A. Salat for their collaboration in the fieldwork. We also thank C. de Jover and J. Mederos for their help in sorting and identifying insects. This research was funded by the project “Agricultural intensification, biodiversity and pollination functioning in the Mediterranean region. Development of environmentally friendly farming schemes” (CGL2012-39442) from the Spanish Government, as well as by an FPI-MEC grant (BES-2013-064829) to MMG. PB was supported by the German Research Foundation (DFG BA4438/2-1) and by the Economic Development and Innovation Operational Programme of Hungary (GINOP-2.3.2-15-2016-00019).
CONCLUSIONS AND MANAGEMENT IMPLICATIONS
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Table S1. Proportion of organically managed arable land (POL) for each selected field.
Locality Local land use and management POL Cabrianes Organic cereal 7.53
Organic cereal 5.96 Conventional cereal 7.60 Conventional cereal 0.19
Legume 2.47 Cardona Organic cereal 28.03
Organic cereal 13.30 Conventional cereal 14.21 Conventional cereal 10.09
Legume 22.72 L’Espunyola Organic cereal 48.03
Organic cereal 65.91 Conventional cereal 30.70 Conventional cereal 66.89
Legume 66.19 Legume 65.05
Gallecs Organic cereal 20.41 Organic cereal 40.28 Organic cereal 72.64 Organic cereal 15.99
Conventional cereal 40.66 Conventional cereal 47.39 Conventional cereal 18.02 Conventional cereal 20.93
Legume 10.15 Legume 2.63 Legume 20.64
Moià
Organic cereal 48.51 Organic cereal 79.26
Conventional cereal 7.38 Conventional cereal 26.74
Legume 79.60 Legume 49.28
SUPPLEMENTARY MATERIAL
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Table S2. The effect of local land use and management (conventional cereal fields, organic cereal fields, and legume fields) as an ordered factor variable on the local flower cover (%) and the fruit sets of Raphanus sativus and Onobrychis viciifolia.
Local land use and management
Local flower cover
Fruit set of Raphanus sativus
Fruit set of Onobrychis viciifolia
Est. ± Std. Error Est. ± Std. Error Est. ± Std. Error Linear term 0.23±0.06*** 0.38±0.06*** 0.39±0.05*** Quadratic term -0.06±0.05 0.08±0.06 -0.01±0.05
*P<0.05; **P<0.01; ***P<0.001
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Figure S1. Initial complete SEM model for the fruit set of Raphanus sativus (Fisher’s C statistic: C = 0.59, p = 0.744). Unstandardised path coefficients are shown for the binomial fruit set model, standardised path coefficients for the bee abundance model, and Pearson’s r correlation coefficients for the correlation between the POL and local variables (local flower cover and local land use and management). Marginal and conditional R2 values are shown for each response variable. Dotted lines represent non-significant effects. The width of each arrow is proportional to the path coefficients. POL = proportion of organically managed arable land.
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Figure S2. Initial complete SEM model for the fruit set of Onobrychis viciifolia (Fisher’s C statistic: C = 0.59, p = 0.74). Unstandardised path coefficients are shown for the binomial fruit set model, standardised path coefficients for the bee abundance model, and Pearson’s r correlation coefficients for correlation between the POL and local variables (local flower cover and local land use and management). Marginal and conditional R2 values are shown for each response variable. Dotted lines represent non-significant effects. The width of each arrow is proportional to the path coefficients. POL = proportion of organically managed arable land.
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Agricultural intensification at field and landscape levels affects flower visitors’ communities through changes in plant communities and their flower traits Marian Mendoza-García, Francesco de Bello, José M. Blanco-Moreno, Lourdes Chamorro, Jan Lepš, Laura Armengot, Berta Caballero-López, F. Xavier Sans En fase de preparación para su envío a Landscape Ecology
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Context
In response to the biodiversity decline caused by agricultural intensification,
it is needed to understand how the changes in functional traits of plant
communities may affect ecosystem functions and services, particularly those
exerted by the fauna that depend on these communities.
Objectives
Our study analyses compositional changes in plant and flower visitor
communities in response to agricultural intensification at field and landscape
levels, and how does the insect community relate to the community-weighted
mean (CWM) of flower traits.
Methods
We evaluated plant and insect assemblages and traits of plant communities,
along a gradient of increasing agricultural land use at landscape level, and
under managements differing in intensity and flower rewards for two years in
northeast Spain.
Results
Plant species composition and the CWM in field centre responded to field
management, whereas in the margin depended on the percentage of arable
land (PAL). Flower visitor composition only responded to the PAL and to
plant composition in the margin. Flower visitor community response to
specific flower traits was consistent among years. Flower colour and
flowering onset affected the composition of insect assemblages in the margin
and flower size in the centre.
Conclusions
Agricultural intensification at both levels affected plant and flower visitor
community trough changes in flower traits. Farming practices and landscape
management can thus affect specific associations between plant and flower
SUMMARY
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visitor communities which have repercussions for biodiversity maintenance
and pollination services in agricultural landscapes.
Keywords
Agricultural intensification, flower traits, flower visitors, species
composition, wildflower resources
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Agricultural intensification at different spatial scales is a major driver of
biodiversity loss in agricultural landscapes (Benton et al. 2003; Tscharntke et
al. 2005; Armengot et al. 2011). Intensification at landscape scale has caused
changes in the structure and composition of the landscape, through the
substitution of most natural habitats with arable fields leading to large,
uniformly-cropped areas, with low spatial heterogeneity. Intensification at
field scale occurs by use of a high amount of external inputs (chemical
fertilisers and pesticides), intensive soil tillage and simplification of crop-
rotational schemes resulting in weed communities with low diversity in-
fields and in neighbouring field margins (Kleijn and Sutherland 2003;
Tscharntke et al. 2005). These changes in landscape structure and land-use
affect insect biodiversity, which provides pollination services both in
agricultural crops and wild plants (Kremen et al. 2007).
Plant-insect interaction also depends on the farming system in
agricultural landscapes (Power and Stout 2011). Organic farming, as an
environmentally friendly farming system, limits the use of fertilisers and
pesticides, and includes crop rotations and green manures (Reganold and
Wachter 2016). In contrast to conventional farming, organic farming should
support high levels of species diversity, and high plant abundance as well,
which in turn can benefit the abundance and diversity of pollinators
(Holzschuh et al. 2008; Rundlöf et al. 2010). Likewise, organic farming
includes crop diversification and the use of nitrogen-fixing crops, such as
legumes (Reganold and Wachter 2016). The implementation of these crops
can also support the pollinator community, through the provision of floral
resources within the crop.
Recently, the approaches based on functional traits have been
suggested as a way to understand the effects of farming practices and of
environmental conditions on the ecosystem services provided by the plant
INTRODUCTION
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communities and generalize results beyond specific taxa (Wood et al. 2015).
This approach has the potential to link ecosystem processes across different
spatial scales and different trophic levels (Lavorel et al. 2013; Carmona et al.
2016). Several studies have shown that plant community diversity and some
of their response functional traits (sensu Lavorel and Garnier 2002; e.g. life
form, specific leaf area, canopy height) are affected by agricultural
intensification in Mediterranean arable landscapes (José-María et al. 2011;
Guerrero et al. 2014; Solé-Senan et al. 2017). However, the effect of flower
traits of plant communities on the assemblage of flower visitors remains still
unclear. Visual flower traits allow deepening into flower visitor patterns and
their interactions with plant community. Visual flower traits are relevant for
the attraction of pollinators (Waser 1983), and they can be associated with
specific flower visitor types (Faegri and Van Der Pijl 1979). For instance,
bumblebees were related with tubular flower plants, whereas hoverflies were
associated with open (Fontaine et al. 2006) and short corolla flower plants
(Campbell et al. 2012). Certain flower traits, such as flower colour, are
considered a good predictor of the prevalence of specific pollinator groups at
high taxonomic levels (e.g. between bees, flies, beetles; McCall and Primack
1992), while others, e.g. flower rewards, can be useful to differentiate
between lower taxonomic levels (Fenster et al. 2004). In this context, various
frameworks have been proposed to analyse the impact of agricultural
practices on functional structure of plant communities, and how these
changes affect ecosystem functions and services (Lavorel and Garnier 2002).
Some flower traits related with insect pollination are affected by the
landscape heterogeneity in agricultural systems (Solé-Senan et al. 2017). For
instance, sown wildflower strips are incorporated in many European
countries to enhance farmland biodiversity. They consist in wildflower seed
mixtures, which can vary their composition and management depending of
the country where they are implemented (Haaland et al. 2011). For instance,
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Jönsson et al. (2015) showed that bumblebees and hoverflies were benefited
at field and landscape levels by the flower strips. Therefore, the selection of
species based on their functional traits can enhance certain groups of insects,
which in turn can improve the delivery of ecosystem services such as
pollination (Wäckers and van Rijn 2012).
The effects of plant community on ecosystem functioning are mainly
determined by the traits of the dominant species (see the ‘mass-ratio
hypothesis’; Grime 1998). Therefore, it should be possible to portray the
changes in ecosystem functions and services by means of the changes in
community-weighted mean (CWM, Garnier et al. 2004; Violle et al. 2007).
Recently, Fornoff et al. (2017) showed that pollinator visitation frequency
and pollinator richness were affected by the CWM of floral traits, such as
rewards, flower height and inflorescence area, reflectance and chemical
traits. Similarly, Robleño et al. (2017) analysed the relationship between the
landscape structure and field management on the CWM response of floral
traits (e.g. corolla shape) to predict, in turn, the response of pollinators.
However, to our knowledge, this is the first study evaluating the direct effect
of CWM floral traits on the composition of the main groups of flower
visitors (Apoidea, Coleoptera and Diptera) in the plant communities in
agricultural landscapes.
In this study we analysed the compositional changes in plant and
flower visitor communities along agricultural intensification gradients at
field and landscape levels in two years. The response of three flower traits
(flower size, flower colour and flowering onset) to the referred
intensification gradients was also analysed. In addition, we evaluated the
relationship between the plant and flower visitor community composition,
and the response of the flower visitor community (Apoidea, Coleoptera and
Diptera) to the CWM of the flower traits selected. We hypothesize that the
percentage of arable land (intensification at landscape level) and the
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management (intensification at field level: organic vs. conventional) and crop
type (cereal vs. legume) affect the plant composition and the CWM of flower
traits and flower visitor composition. We also predicted that the CWM of
flower traits drives the response of flower visitor community. However,
these responses should vary among Apoidea, Coleoptera and Diptera flower
visitors.
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Study design
We reanalysed the data obtained in two samplings to evaluate the effect of
the agricultural intensification in a region dominated by dryland cereal
cropping systems in northeast Spain, one conducted in 2013 (41.75°-
42.05°N; 1.56°-2.21°E) and the second one in 2015 (41.53º-42.05ºN; 1.58º-
2.23ºE) (Figure 1a, see Appendix S1 in Supporting Information).
Sampling 1
In the first sampling year (2013), we selected ten landscapes in an area
characterized by a gradient in agricultural land use. Land use intensity in
each landscape was measured using the percentage of arable land (PAL) in
areas of 500 m radius (mean ± SD = 57.93 ± 15.77; min = 31.13; max =
88.83). The set of landscapes covers an approximate area of 54 × 34 km. In
each landscape, we selected two cereal fields differing in their level of
management intensity (organic vs. conventional), aiming at detecting the
effects of decreasing crop management intensity on flower visitors through
increased plant diversity and flower resource availability. Insecticides are
very rarely used in cereal crops in northeaster Spain; however, herbicides are
routinely applied by farmers in conventional arable crops. Additionally, we
selected legume fields to evaluate the effect that crops have on flower
visitors’ abundance, as such crops can provide additional flower resources.
The studied legume fields were only managed under organic farming,
because legumes are not commonly included in crop rotation of conventional
farms. For that reason, we could not find legume fields in two of ten
landscapes. We evaluated the centre and the margin of each studied field
(Figure 1b).
MATERIAL AND METHODS
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Sampling 2
In the second year (2015), we selected other five landscapes differing in their
proportion of organically managed arable land to test the landscape-scale
effects of organic farming on the abundance of flower visiting insects. The
set of landscapes covers an approximate area of 46 × 54 km. We calculated
the percentage of arable land (PAL) in a radius of 500 m per field (mean ±
SD = 85.11 ± 14.78; min = 50.66; max = 99.99). Within each landscape we
selected two organic and two conventional cereal fields, plus two legume
fields. We included legumes under conventional or organic management, but
we could not find two legume fields in two of five landscapes. This design
only considered the field margin (Figure 1b).
The organic fields selected in both sampling years were managed
according to organic farming European’ regulations (European Union 2007)
by at least 10 years. We used the spatial data from the Spanish Agricultural
Geographic Information System (SIGPAC). All GIS operations were
conducted on ArcGIS 10.2.2 (ESRI 2010).
Fig. 1. (a) The studied localities surveyed in 2013 and 2015, represented by triangles and crosses, respectively, situated in Catalonia, Spain in cereal cropping landscapes (dark grey – arable fields, light grey – other habitats). (b) Schematic representation of 2013 and 2015 surveys. In each transect, located in the margin or in the centre of the studied fields, we placed one pan trap.
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Wildflower resource evaluation
We evaluated the species richness and abundance of flowering plants in the
studied fields. During the first sampling year, the abundance was assessed six
times by counting the number of open flowers per species (between May to
June 2013), in three parallel transects of 1 × 10 m. Each transect was located
at the field margin, at the crop edge (first meter of the crop) and 20 m inside
the field. The surveys were conducted at intervals of 7 to 15 days, depending
on weather conditions. In the second sampling year, we evaluated the
abundance of wildflower resources by visual estimation of the relative cover
of flowers (expressed as percentage over total transect area). Transects were
surveyed once a week for five weeks (between May to June, 2015). The
abundance was evaluated in two parallel transects of 1 × 16 m, one at the
field margin and one at the crop edge.
In each year, the data collected in field margin and edge was
averaged as one transect (hereinafter referred to as "margin"). The
wildflower resources (number of flowers per species or species cover
abundance) in both sampling years were calculated as the mean of all species
flower over the surveys. All plants were identified to species level.
Flower visitor evaluation
Simultaneously to the plant sampling, we surveyed the abundance of flower
visitors using pan traps in both years. These traps were located 1 m above the
ground and consisted on three plastic cups (500 mL, 160 mm diameter)
painted with blue, yellow and white UV reflecting spray. We filled the traps
with water and a small drop of detergent to reduce surface tension. In the
sampling conducted in 2013, pan traps were placed in the margin and the
centre of each studied field, whereas in 2015 only in the field margin (Figure
1b). In both samplings, the traps were exposed for 12 hours, one day per
survey. Surveys were performed under favourable weather conditions (no
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rain, low wind speeds, and diurnal temperatures above 18 ºC). Samples were
stored in 70% alcohol, and specimens of Hymenoptera, Coleoptera and
Diptera were identified to family level. By means of literature (Willemstein
1987; Oosterbroek and Hurkmans 2006) and specialist support, we selected
the families that interact with the plant community and can be considered
flower visitors.
Selection and evaluation of flower traits
Two representative traits related to plant strategy for flower visitor attraction
and one trait related to temporal availability of resources were selected.
These traits were flower size (cm), flower colour (blue, green, pink, purple,
red, violet, white, yellow and various colours) and flowering onset (month).
We considered the diameter of the corolla or the capitulum (species of the
Asteraceae family) to represent the size of the flower. Plant traits data were
extracted from BiolFlor (Klotz et al. 2002) and “Tela Botanica”
(http://www.tela-botanica.org/page:eflore) databases for the 171 species
recorded (see Table S1 for the most common ones). Changes in mean trait
values along the agricultural land use gradients was quantified using CWMs
(Ricotta and Moretti 2011). CWM indicates the average trait value weighted
by the number of flowers per species (sampling 1) or species cover
abundance (sampling 2). Categorical traits were included as dummy variable
to compute the CWM. We can safely discard intrinsic correlations among
traits; only one out of the 55 correlations had r values higher than 0.5 (Table
S1).
Statistical analysis
First, we performed redundancy analyses (RDA, van den Wollenberg 1977)
to explore the response of the plant community composition, CWM of flower
traits and flower visitor community composition to the percentage of arable
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land (PAL) and the crop type and management intensity in both years. RDA
is a constrained ordination method that can be used to test the relationships
between community composition and a set of explanatory variables (i.e.
environmental variables). For the compositional data (i.e. flower or insect
composition) the RDA was used without standardization, for the general data
(i.e. CWM, which are measured at different scales), the response variables
were centered and standardized (ter Braak and Šmilauer 2012). In the first
sampling year, we compared the response variables in relation to the level of
management intensity (organic vs. conventional), crop type (cereal vs.
legume) and different positions (margin vs. centre). For the second sampling,
we evaluated the level of management intensity (organic vs. conventional)
and the crop type (cereal vs. legume). Also, the variance partitioning
procedure was performed by means of RDA (Borcard and Legendre 1994;
Legendre et al. 2005). This method was used to quantify the relative
importance of the landscape (PAL) and the variables at field scale (crop type
and management) on the plant species composition, CWM of flower traits
and flower visitor composition.
Second, the relationship between the plant community composition
and flower visitor community composition was assessed using Co-
Correspondence analysis (CoCA, see Schaffers et al. 2008; ter Braak &
Schaffers 2004). This method directly relates two community compositions
by maximizing the weighted covariance between weighted average species
scores of one community (plants) and weighted average species (families, in
our study) scores of the other community (flower visitors). We conducted
separated models for each year (2013 and 2015) to analyse the relationship
between both plant and pollinator communities within each sampling period.
Finally, we evaluated the effect of CWM of the selected flower traits on the
flower visitor community composition using RDA. We tested separately the
studied positions (margin vs. centre) in the fields selected in 2013, and only
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field margin in 2015. The aim of this analysis was to evaluate the functional
role of the CWM floral traits of wildflower resources on the flower visitor
composition. Therefore, legume fields were removed from this analysis to
evaluate the effects of wildflower resource avoiding the undue effect of the
legume crops.
A log transformation was applied to plant species composition
(number of flower and percentage cover), CWM of flower traits and flower
visitor composition, to achieve normality. Statistical analyses were
performed with CANOCO 5.0 for Windows (Microcomputer Power, Ithaca,
NY, US).
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Plant species composition in the field centre and margin vary in relation to
surrounding landscape and crop type, but the importance of those factors in
the different field positions differ in relation to landscape structure (i.e. the
percentage of arable land or the proportion of organically arable land). The
plant species composition recorded in the field centre in 2013 differed along
the gradient of PAL, and depending on the crop type (Table 1). In 2015, the
plant species composition in the field margin differed along the gradient of
PAL (Table 1). For instance, in the field margin the dominant species
Calendula arvensis and Sonchus oleraceus were more abundant in areas with
lower PAL (plant species composition shown in Figure 2b). We found that
PAL affected significantly CWM of flower traits in field margins (2013 and
2015), whereas in field centre CWM was affected by the intensity of
management (Table 1). Finally, the flower visitor composition both in field
margin and centre differentiated always only along the PAL gradient (Table
1). For instance, in field margin Apidae (Apoidea) and Chloropidae (Diptera)
families were more abundant in areas with higher PAL (flower visitor
composition shown in Figure 2b). The results of the variation partitioning
analysis showed that the overlap of variation explained by PAL and crop
type was very low (which is to a large extent because we have nearly
orthogonal design, i.e. the same representation of field types in all the
landscapes). In comparison of explanatory power of PAL vs. crop type and
management, we should keep in mind that PAL has always just 1 df, whereas
management and crop type have 2 df. Despite this, PAL explained much
more variability in flower visitor composition in all the types and in both the
years, and similarly in CWM of flower traits in field margins. On the
contrary, in the field centre, the management has higher explanatory power,
both for the CWM and for the species composition (Table S2).
RESULTS
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Table 1. Redundancy analysis (RDA) of the plant species composition, community weighted mean (CWM) values of flower traits and flower visitor composition collected in each year, with environmental factors (% arable land, intensity of management: organic vs. conventional, and crop type: cereal vs. legume) as explanatory variables. We conducted a RDA with a forward selection separately for each year and field position. *P<0.05; **P<0.01 Only significant fractions are reported.
Environmental variables
Plant species composition
CWM flower traits
Flower visitor composition
Explains (%)
pseudo-F
Explains (%)
pseudo-F
Explains (%)
pseudo-F
2013
cent
re
Percentage of arable land
1.9*
3.2**
Crop type
2.0*
Management
2.5**
mar
gin
Percentage of arable land
2.2*
1.9*
Management
2015
mar
gin
Percentage of arable land
1.8*
1.9*
10.2**
Crop type
Management
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Co-correspondence analysis (CoCA) showed that the plant and the
flower visitor communities were not correlated which each other in the field
centre in the first sampling year (2013, Table S3). In contrast, the plant and
the flower visitor communities were significantly correlated in the field
margin in both sampling years (Table S3, Figure 2), indicating that the
communities changed in concert. Nevertheless, the amount of variation (i.e.
total inertia; Table S3) in the communities was much larger than the
variation captured by CoCA (i.e. total variation; Table S3).
The flower visitor community (Apoidea, Coleoptera and Diptera)
was also explained through the CWM of the selected plant floral traits (Table
2). In the field centre, the CWM of flower size explained the Diptera
composition. For instance, large flower size favoured Bibionidae family, but
not Syrphidae family. In the field margins evaluated in 2013 and 2015,
CWM of flower colour and flowering onset influenced Apoidea, Coleoptera
and Diptera composition. Apoidea composition (2013) was explained by red
flower colour, favouring Megachilidae family. Purple and pink flower
colours explained Coleoptera composition in the first year (2013), whereas
violet flower colour and flowering onset explained it in the second year
(2015). For instance, purple, pink and violet flower colour correlated
positively with Malachiidae, Nitidulidae and Scarabaeidae families,
respectively. Diptera composition was explained by green flower colour in
both years. This flower colour favoured Chloropidae family, but not
Syrphidae family. In addition, Diptera composition was also explained by
flowering onset in 2015. For instance, an early flowering onset favoured
Syrphidae family.
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Fig. 2. Co-correspondence analysis (CoCA) with the first two axes and 25 plant species (left-hand subplot) in the field margin and 25 flower visitor families (right-hand subplot) with highest average abundance, corresponding to the samplings conducted in (a) 2013 and (b) 2015. The environmental descriptors are passively projected into the left-hand subplot. Plant species and flower visitor family abbreviations are given in Table 4S and 5S, respectively.
-1.5 1.0
-0.8
1.0
% Arable land
Conventional cereal
Organic cereal
Cap_bur Con_arv
Dip_eru
Ech_vul
Fum_off
Fum_par
Gal_apa
Gal_luc
Gal_spu
Gal_tri
Mal_syl
Med_pol
Med_sat
Pap_rho
Pol_avi Sca_pec
Ste_med
Tor_arv
Tri_cam
Ver_arvVer_hed
Ver_per
Vic_cra
Vic_sat
Vio_arv
-1.5 1.0
-0.8
1.0
Ant Bib
Cal
ChlHyb
Mus
Pho
Sar
Sca
Sci
Sep
Syr
Tac
Bup
Cer
Chr
DasMal
Mor
Nit Oed
Sca
And
ApiHal
-1.5 1.0
-2.0
1.0
% Arable land
Conventional cereal
Organic cereal
Ana_arv
Ana_cla
Bal_nig
Bor_off
Cal_arv
Car_ten
Con_arvDip_eru
Eup_serFum_off
Gal_apaGal_luc
Mal_syl
Mar_vul
Med_polPap_rho
Pol_aviPol_con
Pot_rep
Sil_mar
Son_ole
Tor_arv
Ver_per
Vic_vil
Vio_arv
-1.5 1.0
-2.0
1.0
Bup
Cer
ChrDas
Mal
Mor
Nit
Oed
Sca
Agr
Ant
Chl
Hyb
Mus
Pho
Sar
Sca
Sci
Sep
Syr
Tac
Uli
And
Api
Hal
2015
2013
Plant species composition Flower visitor composition
(a)
(b)
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Table 2. Redundancy analysis (RDA) of the flower visitor composition for each order separately collected in cereal fields during both years, with community weighted mean (CWM) values of flower traits as explanatory variables. RDA with a forward selection was conducted in each year and field position. *P<0.05; **P<0.01 Only significant fractions are reported.
Flower visitor composition within groups
CWM flower traits
2013 2015 Centre Margin Margin
Explains (%)
pseudo-F
Explains (%)
pseudo-F
Explains (%)
pseudo-F
Apoidea Red colour
6.0**
Coleoptera Pink colour
2.9*
Purple colour
3.5*
Violet colour
4.5*
Flowering onset
7.3*
Diptera Green colour
2.5*
3.2*
Flowering onset
3.3*
Flower size
2.3*
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Effects of agricultural intensification at different spatial scales
Several studies have shown that complete understanding of biodiversity
patterns in agricultural landscapes requires their evaluation at multiples
scales (Tscharntke et al. 2005; Concepción et al. 2008). Our study shows that
the plant composition and the CWM flower traits in the field margin
responded to the landscape variables, as measured by PAL, whereas in the
field centre their response is more dependent on local characteristics, i.e. on
farming practices at field level. Our results are consistent with the findings of
Guerrero et al. (2014), who showed that the response of plant traits in field
centre is driven by agricultural intensification at field but not at landscape
scale. José-María et al. (2011) found that species plant composition can be
affected more by farming practices and field position than by the surrounding
landscape. Soil disturbance can affect plant species composition in the field
centre, whereas the simplification of landscape complexity can influence the
plant composition in field margins (José-María et al. 2011; Solé-Senan et al.
2014). Our results thus support that the farming practices have a higher effect
in the field centre than in the field margin.
Despite the different effects of PAL and farming practices on the
plant species composition and the CWM traits in the field centre and margin,
the flower visitor composition was affected by PAL independently of the
position within the field. This reflects the ability of insects to spill-over from
the field margin to the field center diluting the effect of farming position.
According to Batáry et al. (2011), the response of flower visitors to the
management intensity is moderated by the landscape. The landscape
structure can influence on the availability of food and nesting and mating
habitats, which are required by flower visitors (Kremen et al. 2007). For
instance, Andersson et al. (2013) found that the species composition of
pollinator communities was modified by the landscape homogeneity, mainly
DISCUSSION
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caused by agricultural intensification. Similarly, the species composition of
some beetle assemblages was modified by the agricultural land use at
landscape scale (Cole et al. 2002). Our results suggest that environmental
measures at landscape scale (PAL) can affect the flower visitor community,
which support the maintenance of ecosystem services, such as pollination
(e.g. Batáry et al. 2013).
Relationships between plant composition and flower visitor communities
Our study indicates that plant species composition in the field margin
influenced the flower visitor composition in both sampling years. Some
studies have shown that the reproductive success and persistence of plants
can be affected by the diversity and community composition of flower
visitors (Fontaine et al. 2006; Albrecht et al. 2012), but also plants influenced
the flower visitor community (Mayer et al. 2011). For instance, Schaffers et
al. (2008) showed that the plant species composition thriving in a grassland
is the most effective predictor of arthropod assemblage composition, which
included bees, hoverflies and some beetle families. Our research also shows
that the plant species composition located in the field centre did not affect the
flower visitor composition. This result might be related with the lower
abundance of plant and flower visitor in the field centre compared with the
margin. For instance, the abundance of Apoidea and Coleoptera were 1.8 and
2.2 times lower in the field centre than in the margin, respectively (data not
shown). In addition, the spatial and temporal arrangement of flowers in the
plant community can influence the insect visits (Thompson 2001). We
suggested that the simplification of landscape can have an indirect effect on
flower visitor composition, via changes in plant composition in the field
margin in agricultural landscapes.
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Effects of CWM flower traits on flower visitor composition
The wildflower resources characterized by the CWM flower traits influenced
the flower visitor community located in the centre and the margin of studied
fields. As we hypothesized, each group of the flower visitor community
(Apoidea, Coleoptera and Diptera) had a different response to CWM flower
traits. The differences in floral design (e.g. size, morphology, colour, floral
rewards) and floral display (e.g. arrangement of inflorescence) determine the
success of insect foraging on a specific flower type (Goulson 1999), but this
choice can also be based in multiple flower traits (Hegland and Totland
2005).
Although the composition of plant and flower visitor communities
varied in response to the factors considered among years, the flower visitor
community response was maintained for specific flower traits. The flower
colour affected the flower visitor composition in the field margin, whereas
the flower size influenced the composition in field centre. According to
colour preferences described in pollination syndromes, bees and coleopterans
prefer blue and white flowers, respectively, and flies are more attracted by
yellow and white flowers (Faegri and Van Der Pijl 1979). CWM is more
influenced by traits of dominant plants; therefore, this could be the main
reason because the CWM colours of flowers that correlate with the main
axes of variation of flower visitor community composition do not coincide
with the ones reported in the literature. However, we also found some
indications that there is a linkage between flower colour and some elements
of the insect community. For instance, some families of Apoidea responded
to red flower colour, which in our sampled fields correspond to species that
are classified as flowers pollinated by hymenopterans, according to BiolFlor
database. We also observe a biological significance pattern, as families of
different groups of flower visitors have similar responses to the same flower
colours in both sampling years. In a study that also evaluated the CWM
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colour of flowers, Fornoff et al. (2017) showed that the green reflectance was
negatively correlated with species richness and visitation frequency,
particularly of bees, which was the pollinator group more diverse and with
higher visitation rates. However, other studies indicated contrasted
relationships, as e.g. Reverté et al. (2016) did not find a relationship between
the pollinator composition and the flower colour in some Mediterranean
communities (grasslands and scrublands), suggesting that the same corolla
colour may attract different pollinators. Moreover, they also suggested that
other flower traits as the floral rewards or the corolla depth can influence the
preferences of pollinators. Our findings showed that flower visitor
composition (Coleoptera and Diptera) did not only respond to the flower
colour, but also to the flowering onset in the field margins of the second
year. For instance, Guerrero et al. (2014) found that management
intensification promotes an earlier flowering in the arable plant communities,
probably as early flowering species may avoid the stronger negative effects
of crop competition. In this sense, some flower visitors can respond to this
pattern, and they may be attracted by plant species with an earlier flowering.
Our results also showed that the composition of Diptera assemblage
responded to the flower size of the dominant plants in the field centre (e.g.
Bibionidae correlating with larger flowers). The flower size can affect the
attractiveness of a plant for pollinators, varying the rates of visitations
(Stanton 1987; Elle and Carney 2003). Some studies have demonstrated a
discrimination of the pollinators based on flower size, which preferred the
population with the largest flowers (Elle and Carney 2003; Kennedy and Elle
2008). This pollinator preference can be caused by the positive correlation
between the corolla width and the floral reward (Kennedy and Elle 2008). In
addition, in the field centre, the wildflower resources are surrounded by
cereal crops, therefore, a large flower size also may increase the flower
visibility for flower visitors, which concentrate their activity in field margins.
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Agricultural intensification at field and landscape levels interacts with the
plant and flower visitor community and the CWM of flower traits. On the
one hand, the field management should be considered in the plant
conservation measures in Mediterranean arable landscapes, promoting low-
intensity agricultural practices. On the other hand, environmental measures at
landscape level must be considered to promote the maintenance of ecosystem
services mediated by the flower visitor community, such as pollination.
Some measures may include the creation of landscape features such as field
margins. However, all flower visitors did not respond uniformly to plant
community traits. Therefore, a previous selection of the plant species based
on their flower traits is recommended, to develop the field margins that
support the conservation of specific flower visitors and, in turn, sustain the
pollination services in highly intensified agricultural landscapes.
Acknowledgements
This research was funded by the project “Agricultural intensification, biodiversity and pollination functioning in the Mediterranean region. Development of environmentally friendly farming schemes” (CGL2012-39442) from the Spanish Government, as well as by an FPI-MEC grant (BES-2013-064829) to MMG. We are very grateful to the farmers who allowed us to use their fields, and several students for their collaboration in the fieldwork. We also thank J. Mederos and A. Viñolas from the “Museu de Ciències Naturals de Barcelona” for their help in sorting and identifying insects.
CONCLUSIONS AND MANAGEMENT IMPLICATIONS
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SUPPLEMENTARY MATERIAL
Tab
le S
1. R
esul
ts o
f P
ears
on c
orre
lati
on c
oeff
icie
nts
amon
g co
mm
unit
y-w
eigh
ted
flow
er tr
ait v
alue
s ob
tain
ed in
bot
h sa
mpl
ing
year
s (2
013
and
2015
).
F
low
er
size
F
low
erin
g
onse
t B
lue
co
lour
G
reen
co
lour
P
ink
co
lour
P
urpl
e
colo
ur
Red
co
lour
V
ario
us
colo
urs
Vio
let
colo
ur
Whi
te
colo
ur
Flo
wer
ing
onse
t -
0.42
2**
B
lue
colo
ur
0.02
7
-0.4
17**
G
reen
col
our
-0.1
10
0
.051
-0
.130
Pin
k co
lour
-0
.175
0.
021
-0.1
63
-0.0
54
Pur
ple
colo
ur
0.19
9 -0
.104
-0
.149
-0
.058
-0
.206
Red
col
our
0
.757
**
-0.2
08
-0.1
54
-0.1
76
-0.2
02
0.01
5
V
ario
us c
olou
rs
0.08
4 -0
.013
0
.125
-0
.048
0
.113
-0
.001
0.
071
V
iole
t col
our
0.01
3 -0
.063
-0
.018
0
.163
0
.034
-0
.215
-0
.061
-0
.073
W
hite
col
our
-0
.444
**
0
.405
**
-0.1
50
-0.1
00
-0.2
00
-0
.355
**
-0.
270*
-0
.180
-0
.156
Yel
low
col
our
-0.1
19
0.0
45
-0.2
23
0.1
51
0.0
95
-0.2
74*
-0.1
29
-0.1
65
0.15
5 -0
.368
**
Sig
nifi
canc
e le
vels
are
as
foll
ows:
* p
< 0
.05
and
** a
nd p
< 0
.01
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141
Tab
le S
2. V
aria
tion
par
titio
ning
of
the
vari
ous
uniq
ue f
ract
ions
(ou
tsid
e of
the
cir
cles
’ in
ters
ecti
on,
a an
d b)
and
ove
rlap
(i
nsid
e th
e in
ters
ecti
on,
c ) o
f th
e ef
fect
of
diff
eren
t ex
plan
ator
y va
riab
les
(PA
L a
nd c
rop
type
and
man
agem
ent)
on
plan
t co
mpo
siti
on, c
omm
unit
y w
eigh
ted
mea
n (C
WM
) va
lues
of
flow
er tr
aits
and
flo
wer
vis
itor
com
posi
tion
.
Pl
ant
com
posi
tion
CW
M
flow
er tr
aits
Fl
ower
vi
sito
r co
mpo
sitio
n
a
c b
a c
b a
c b
2013
Fie
ld c
entr
e 0.
063
0.00
5 0.
111
0.05
1 0.
008
0.12
8 0.
122
0.00
0 0.
075
Fie
ld m
argi
n 0.
059
0.00
0 0.
047
0.11
8 0.
000
0.03
3 0.
099
0.00
6 0.
040
2015
Fie
ld m
argi
n 0.
054
0.00
2 0.
062
0.05
4 0.
000
0.04
1 0.
261
0.00
0 0.
050
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142
Tab
le S
3. R
esul
ts o
f co
-cor
resp
onde
nce
anal
yses
(C
oCA
) te
stin
g co
rrel
atio
ns b
etw
een
plan
t an
d fl
ower
vis
itor
com
mun
ity
com
posi
tion
for
eac
h sa
mpl
ing
year
(20
13 a
nd 2
015)
. C
ross
-cor
r. a
xes
1 an
d 2
repr
esen
t th
e cr
oss-
corr
elat
ion
betw
een
the
firs
t an
d se
cond
Co-
CA
axe
s, r
espe
ctiv
ely;
tot
al i
nert
ia r
epre
sent
s th
e am
ount
of
vari
atio
n in
eac
h co
mm
unit
y; e
xpla
ined
va
riat
ion
repr
esen
ts t
he a
mou
nt o
f va
riat
ion
expl
aine
d by
all
Co-
CA
axe
s; F
ist
axis
lam
bda
(p-v
alue
) re
pres
ents
the
tes
t st
atis
tic
and
p-va
lue
for
test
ing
the
cros
s-co
rrel
atio
n be
twee
n th
e tw
o co
mm
unit
ies
in t
he f
irst
axi
s. B
old
valu
es r
epre
sent
si
gnif
ican
t val
ues,
P <
0.0
5.
Yea
r Fi
eld
po
sitio
n C
omm
unity
1
Com
mun
ity
2
Cro
ss-
corr
. ax
es 1
Cro
ss-
corr
. ax
es 2
Tot
al
iner
tia
com
m. 1
Tot
al
iner
tia
Com
m. 2
Tot
al
vari
atio
n (a
ll ax
es)
Firs
t axi
s la
mbd
a (p
-val
ue)
2013
C
entr
e P
lant
F
low
er
visi
tor
0.85
0.
83
6.56
0.
87
0.27
0.
061
(0.5
12)
Mar
gin
Pla
nt
Flo
wer
vi
sito
r 0.
95
0.94
4.
64
0.77
0.
20
0.05
2 (0
.004
)
2015
M
argi
n P
lant
F
low
er
visi
tor
0.92
0.
92
7.46
0.
69
0.27
0.
089
(0.0
01)
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Table S4. Plant trait data (selection of the 25 most abundant species) and species abbreviation of wildflower resources surveyed during both years (2013 and 2015). Plants were identified according to de Bolòs et al. (2005).
Species Species abbreviation
Flower Size (cm)
Flowering Onset (month)
Flower colour
Anagallis arvensis L. Ana_arv 0.80 2 Blue
Anacyclus clavatus (Desf.) Pers. Ana_cla 2.50 5 White
Ballota nigra L. Bal_nig 1.43 4 Purple
Borago officinalis L. Bor_off 2.75 2 Blue
Calendula arvensis (Vaill.) L. Cal_arv 2.25 2 Yellow
Capsella bursa-pastoris (L.) Medik. Cap_bur 0.40 1 White
Carduus tenuiflorus Curtis Car_ten 0.85 5 Pink
Convolvulus arvensis L. Con_arv 1.75 4 White
Diplotaxis erucoides (L.) DC. Dip_eru 1.20 1 White
Echium vulgare L. Ech_vul 1.55 2 Pink
Euphorbia serrata L. Eup_ser 0.20 2 Green
Fumaria officinalis L. Fum_off 0.75 2 Purple
Fumaria parviflora Lam. Fum_par 0.55 2 White
Galium aparine L. Gal_apa 0.23 6 White
Galium lucidum All. Gal_luc 0.43 5 White
Galium spurium L. Gal_spu 0.12 5 White
Galium tricornutum Dandy Gal_tri 0.22 5 White
Malva sylvestris L. Mal_syl 4.50 3 Purple
Marrubium vulgare L. Mar_vul 0.65 5 White
Medicago polymorpha L. Med_pol 0.40 2 Yellow
Medicago sativa L. Med_sat 0.90 4 Various
Papaver rhoeas L. Pap_rho 5.50 3 Red
Polygonum aviculare L. Pol_avi 0.35 4 Pink
Polygonum convolvulus L. Pol_con 0.40 5 Green
Potentilla reptans L. Pot_rep 1.75 1 Yellow
Scandix pecten-veneris L. Sca_pec 0.75 2 White
Silybum marianum (L.) Gaertn. Sil_mar 1.60 5 Purple
Sonchus oleraceus L. Son_ole 2.00 2 Yellow
Stellaria media (L.) Vill. Ste_med 0.70 1 White
Torilis arvensis (Huds.) Link Tor_arv 0.35 5 White
Trifolium campestre Schreb. in Sturm Tri_cam 0.42 4 Yellow
Veronica arvensis L. Ver_arv 0.35 3 Blue
Veronica hederifolia L. Ver_hed 0.70 3 Blue
Veronica persica Poir. in Lam. Ver_per 1.05 1 Blue
Vicia cracca L. Vic_cra 1.10 4 Violet
Vicia sativa L. Vic_sat 2.00 4 Blue
Vicia villosa Roth Vic_vil 1.40 3 Violet
Viola arvensis Murray Vio_arv 1.25 4 White
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Table S5. Family abbreviation of flower visitor composition showed in Co-correspondence analysis (CoCA) and total flower visitor abundance collected by pan traps in field centre and margin in both sampling years (2013 and 2015).
Group Family Abbreviation 2013 2015 Centre Margin Margin
Apoidea Andrenidae And 60 32 198 Apidae Api 98 98 444 Halictidae Hal 75 68 487 Megachilidae 6 11 23 Melittidae 2 4 2 Coleoptera Anthicidae 2 2 2 Buprestidae Bup 175 361 471 Cantharidae 40 29 70 Cerambycidae Cer 16 42 76 Chrysomelidae Chr 12 40 80 Dasytidae Das 211 273 889 Malachiidae Mal 78 45 170 Mordellidae Mor 57 294 163 Nitidulidae Nit 905 985 9976 Oedemeridae Oed 49 123 443 Scarabaeidae Sca 525 592 241 Diptera Agromyzidae Agr 34 31 292 Anthomyiidae Ant 2992 1554 3155 Bibionidae Bib 368 124 38 Bombyliidae 70 45 35 Calliphoridae Cal 31 43 19 Carnidae 7 12 39 Ceratopogonidae 2 3 0 Chloropidae Chl 897 302 2673 Conopidae 3 4 36 Empididae 29 32 60 Hybotidae Hyb 267 204 1060 Keroplatidae 0 1 6 Lonchopteridae 0 2 3 Milichiidae 48 10 27 Muscidae Mus 15 33 61 Mycetophilidae 0 2 0 Phoridae Pho 1044 707 4302 Sarcophagidae¡ Sar 69 87 76 Scatopsidae Sca 66 66 132 Sciaridae Sci 555 166 698 Sepsidae Sep 116 115 89 Simuliidae 1 1 1 Stratiomyidae 52 41 22 Syrphidae Syr 130 146 347 Tachinidae Tac 69 88 58 Tephritidae 27 16 11 Therevidae 0 1 1 Ulidiidae Uli 5 2 115
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Patterns of flower visitor abundance and fruit set in a highly intensified cereal cropping system in a Mediterranean landscape Marian Mendoza-García, José M. Blanco-Moreno, Lourdes Chamorro, Laura José-María, F. Xavier Sans Agriculture, Ecosystems and Environment (2018), 254: 255–263
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In intensive agricultural landscapes, decreased pollinator numbers have often
been attributed to the loss of natural habitats. However, several studies show
that certain mass flowering crops, such as oilseed rape (OSR), can alter the
pattern of pollinator abundance at a field and landscape level. These studies
have focused mainly on bees; information about the effect of OSR crops on
other taxa is missing. We evaluated the abundance of bees and other (non-
bee) flower visitors, and the fruit set of insect-pollinated target plants
(Raphanus sativus and Onobrychis viciifolia) on the margins of OSR and
cereal fields in landscapes with varying densities of non-cropped habitats
(landscape structure). The presence of OSR crops and wildflower resources
in field margins had varying effects on the abundance of bees and non-bee
flower visitors. Bee abundance was enhanced by OSR crops, but decreased
in complex landscapes. On the other hand, the abundance of non-bee flower
visitors depended on the landscape structure, particularly on the location of
cereal fields. Despite the numerous and diverse communities of pollinators
attracted by OSR crops and wildflower resources, fruit set was enhanced
only for generalist insect pollinated plant species, because competition
processes for pollinators affect specialist plant species. We conclude that the
incorporation of OSR crops and maintenance of wildflower resources in agri-
environmental schemes should be considered to improve the pollination
services in agricultural landscapes highly dominated by cereal fields.
Keywords: mass flowering crops, bees, non-bee flower visitors, pollination
syndromes, landscape structure, wildflower resources
SUMMARY
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Agricultural intensification is one of the main causes of biodiversity decline
(Matson et al., 1997; Tilman et al., 2001) and disruption of associated
ecosystem services (Kleijn et al., 2009). Agricultural intensification from
within field to landscape levels is generally correlated with the decline of
wild pollinators and the services they provide to crops and wild plants
(Steffan-Dewenter et al., 2005; Biesmeijer et al., 2006; Potts et al., 2010).
Changes in land-use and landscape structure affect the composition of nearby
habitats and pollinators, in turn affecting their interactions at individual,
population and community levels (Kremen et al., 2007).
In agricultural landscapes that are devoted to the production of crops
that do not require insect pollination, such as cereal plantations, the provision
of pollination services to insect-pollinated plants can be compromised. For
example, insect pollinators may depend on the presence of natural and semi-
natural vegetation that provides shelter, nesting sites and food. Pollinators
can be displaced from natural and semi-natural vegetation to cropland if
pollinators benefit from mass flowering crops or wildflower resources
thriving in the field margins (Tscharntke et al., 2012).
For diverse agronomic and economic benefits, mass flowering crops
have been incorporated into crop rotations to break-up the continuous
cultivation of cereals (Pimentel et al., 1997; Klein et al., 2007; Kennedy et
al., 2013). Moreover, these crops can reduce the food resource limitations for
pollinators, thereby supporting pollination services (Westphal et al., 2003;
Diekötter et al., 2010). Oilseed rape (Brassica napus L., OSR) is one of the
most commonly used mass flowering crops because of the demand for its oil
and increasing biofuel demand (FAO, 2015). OSR crops offer a highly
rewarding resource of pollen and nectar that enhance pollinator abundance
(Morandin and Winston, 2005). Most studies have evaluated the effect of
OSR crops on bees, particularly honeybees, which are considered the most
INTRODUCTION
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economically valuable pollinator (McGregor, 1976). Although other
pollinators could also be enhanced by OSR crops in intensive agricultural
landscapes, information about this relationship and about the abundance and
diversity of other taxa remains scarce.
In highly intensified arable landscapes, the presence of patches of
non-cropped habitats, remnants of natural and semi-natural habitats, and the
presence of wildflower resources in the field margins is extremely important
for maintaining pollination services (Banaszak, 1992; Walther-Hellwig and
Frankl, 2000; Garibaldi et al., 2011; Winfree et al., 2011). Several studies
have demonstrated that recurrent resource pulses of mass flowering crops,
such as OSR crops, can be beneficial to pollinators only when natural and
semi-natural habitats are present in agroecosystems (Westphal et al., 2009;
Holzschuh et al., 2013; Diekötter et al., 2014; Riedinger et al., 2015). For
instance, Holzschuh et al. (2013) showed that the abundance of a wild bee
species was enhanced when nesting habitats were present, particularly
depending on the amount of OSR crops. Similarly, some studies proposed
that the establishment of various mass flowering crops together with the
maintenance of semi-natural habitats are effective conservation measures for
maintaining bumblebee populations (e.g. Westphal et al., 2003, 2009).
However, most researchers have studied landscapes where mass flowering
crops are dominant. It is still unknown how discrete areas of mass flowering
crops and wildflower resources at field margins, together with non-cropped
habitats, can affect pollinators in cereal-dominated landscapes.
Plant communities can affect the interactions between any given
plant species and its ensemble of pollinators by reducing the frequency of
pollinators’ visits through competition (Pleasants, 1981) or increasing this
frequency via facilitation (Waser and Real, 1979; Moeller, 2004). As a
consequence, changes in plant communities may strongly affect pollination
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processes by negatively or positively altering the pollinator’s availability and
effectiveness in delivering conspecific pollen.
The vulnerability of plant reproduction to land-use change depends
on such factors as a species reliance on pollinators and the effect of changes
in the surrounding landscape on pollination processes. Species specific plant
traits, including breeding system, specialization of plant pollinator
interaction, and floral traits, strongly influence the likelihood that plant-
pollination interactions are disrupted (Bond, 1995; Aizen et al., 2002;
Vázquez and Simberloff, 2002; Potts et al., 2010), therefore affecting their
sensitivity to land-use changes. Declines in pollination services negatively
affect obligate outcrossing plants, especially insect pollinated plants (Aguilar
et al., 2006). Specialist insect-pollinated species are more vulnerable to
changes than generalist species (Biesmeijer et al., 2006), but the magnitude
of the effects can depend on landscape structure. For instance, some wild
plants can compete with the crop for attention from a limited number of
pollinators in the vicinity of mass flowering crops (Holzschuh et al., 2011).
On the other hand, wild plants can benefit from mass flowering crops if
pollinators do not limit their visits to the most attractive flowers, such as
from crops, but also visit surrounding areas (Rathcke, 1983). For instance,
Hanley et al. (2011) showed an increase of pollination success of wild
margin plants owing to the presence of mass flowering crops. However, to
our knowledge there are few studies that evaluate the impact of mass
flowering crops on generalist and specialist plants species in intensive
agricultural landscapes.
The purpose of this study was to evaluate the effect of the presence
of a neighbouring mass flowering crop (oilseed rape), landscape structure
(represented by the density of non-cropped habitats) and wildflower
resources on the abundance of bees (Hymenoptera: Apoidea) and other
flower visitors (non-bees) and on the fruit set of two target species with
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different pollination syndromes. We also compared the abundance of bees,
non-bee flower visitors and target species (generalist vs. specialist) to
landscape structure. We tested the following hypotheses: (i) availability of
resources provided by OSR crops increases the abundance of both bee and
non-bee flower visitors and the fruit set of target species, (ii) increasing
density of non-crop habitats in the landscape enhances the abundance of bees
and non-bee flower visitors and improves the fruit set of target plants in field
margins near OSR crops, and (iii) the abundance of bees and non-bee flower
visitors increases with wildflower resources, but this effect is negligible in
field margins near OSR crops; therefore, if wildflower resources benefit the
pollination process, this effect is more noticeable in field margins nearby
cereal crops. However, competition and facilitation interactions for resources
coupled with specific pollinator requirements can affect fruit set patterns.
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Study region
The experiment was conducted between April and June of 2014 in Catalonia,
Spain (41° 48′–41° 40′ N; 1° 14′–1° 28′ E) (Fig. 1). The study area is
primarily devoted to the production of cereals, but it also includes some mass
flowering crops. The natural and semi-natural vegetation is composed of a
complex mosaic of woodlands, which are mainly pines (Pinus nigra Arnold)
but also include evergreen oaks (Quercus rotundifolia Lam.), deciduous oaks
(Quercus faginea Lam.), shrublands and perennial-dominated grasslands.
The remnants of this vegetation are mainly linear features intermingled
between arable fields. Annual mean minimum and maximum temperatures
were 8.3 and 17.4 °C, respectively, and the accumulated annual precipitation
was 631.8 mm. For our study, we chose an area of 20× 15 km with over 75%
of arable land (Fig. 1). Here, we selected 21 margins between oilseed rape
(OSR) and cereal fields and another 21 between cereal (C) fields.
Hereinafter, we call these margins OSR-C and C-C field margins,
respectively. The studied field margins were located at least 400 m from each
other. During the study, the landscape was dominated by cereal crops
(mainly barley and wheat) due to the extremely low rainfall in autumn 2013
that forced farmers to cultivate cereals instead of oilseed rape. Fertilization
was based on pig slurry and mineral fertilizers for both crop types. The OSR
crop fields were treated with insecticides before the onset of the flowering
period. Weed control was conducted in both cereal and oil seed rape fields
by application of herbicides, also during late winter before the onset of crop
flowering. Field edges were regularly managed by application of wide-
spectrum herbicides. These extremely intense farming operations, as well as
the recurrent herbicide deposition into the field margins due to drift, resulted
in species-poor plant communities.
MATERIALS AND METHODS
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Figure 1. The studied oilseed rape-cereal and cereal-cereal field margins, represented by circles and triangles, respectively, were located in Catalonia, Spain in highly intensified cereal cropping landscapes (light grey – arable fields, dark grey – other habitats).
Density of non-cropped habitats
The length of the field-margin network was used as a measure of landscape
structure. Field margins were digitized on orthophotomaps (1:25,000). The
field margins were defined as linear elements composed of natural and semi-
natural habitats. Field margins were digitized as single lines (arcs in GIS
terminology) when margins were narrower than 3 m, whereas patches of
natural and semi-natural habitats wider than 3 m were delineated as surfaces
(polygons in GIS terminology). The sum of all linear elements (all arcs,
irrespective of whether they were single arcs or arcs enclosing polygons)
within a radius of 500 m around each selected field was defined as the
density of non-cropped habitats (ranging from 6.64 to 28.52 km). All GIS
operations were conducted on ArcGIS 10 (ESRI, 2010).
Wildflower resources and OSR flower resources
We evaluated the richness and abundance of plants that produce nectar and
pollen in OSR-C and C-C field margins because the delivery of pollination
services to a target plant depends on the surrounding plant community. The
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surveys were performed once a week for six weeks. During each survey, the
cover of plants in full bloom in three parallel transects of 1 × 12 m in the
study field margins was assessed. The central transect corresponded to the
non-crop vegetation (1 m width) between fields, and the two adjacent
transects corresponded to the first metre of the oilseed rape or cereal field in
the OSR-C field margins or to the first metre of the cereal field in the C-C
margins (Fig. 2). Abundance of wildflower resources was assessed by visual
estimation of the relative cover of flowers in the transect area. All flowering
plants were identified to the species level (according to de Bolòs et al.,
2005). Flower resource and pollinator surveys were evaluated simultaneously
during the OSR blooming period.
Figure 2. Schematic representation of oilseed rape-cereal and cereal-cereal field margins in the study system. In the centre of the central transects, we placed six individuals of each target species (Raphanus sativus and Onobrychis viciifolia) at both sides of a pan trap.
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Bee and non-bee flower visitors surveys
For each field margin, we placed one pan trap consisting of three cups
(500 mL, 160 mm diameter) painted with UV reflecting blue, yellow and
white spray. The use of pan traps is a common passive sampling method
which evaluates the activity density of flower-visiting insects and does not
cause a lasting negative effect on populations (Gezon et al., 2015). Pan traps
were located 1 m above the ground and 1 m apart from each group of target
species (Fig. 2). They were filled with water and a small amount of detergent
to reduce surface tension and were operated for 24 h. The surveys were
performed once a week for six weeks under favourable weather conditions
(no rain, low wind speeds, and diurnal temperatures above 18 °C). Samples
were stored in 70% alcohol, and specimens were identified to the family
level. We evaluated bees (Hymenoptera: Apoidea) and non-bee flower
visitors (specimens of Hymenoptera excluding Apoidea, Coleoptera and
Diptera orders) separately.
Target species
Raphanus sativus L. (Brassicaceae) and Onobrychis viciifolia Scop.
(Fabaceae) were used as target species to assess the fruit set in OSR-C and
C-C margins fields. R. sativus is an annual plant that produces numerous
symmetrical actinomorphic white flowers on a broad-branched inflorescence.
It is self-incompatible (Young and Stanton, 1990) and commonly visited by a
wide array of pollinators, such as honey bees, bumblebees, wild bees,
hoverflies and butterflies (Steffan-Dewenter and Tscharntke, 1999; Albrecht
et al., 2007). The perennial O. viciifolia produces numerous zygomorphic
melliferous pink flowers on several unbranched inflorescences (Kells, 2001).
It is an outbreeding insect pollinated species, almost entirely pollinated by
bumblebees, honey bees, and wild bees (Hayot Carbonero et al., 2011).
Onobrychis viciifolia is considered to be an obligate insect-pollinated species
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(Hanley et al., 2008). To achieve correct zygomorphic flower handling,
pollinators can adopt only a limited number of physical orientations. In
contrast, the simple morphology of actinomorphic flowers facilitates their
handling and promotes visits from a wider variety of pollinators (Wolfe and
Krstolic, 1999). This difference in the diversity of pollinators that can
effectively interact with their flowers, allows the classification of R. sativus
as a generalist insect-pollinated species and O. viciifolia as a specialist
insect-pollinated species.
Fruit set
Seeds of the target species were sown in 5 L pots filled with commercial
garden soil (mixture of peat, vermiculite and clay) under outdoor conditions
at the Experimental Fields Service of the University of Barcelona (January
2014). Six individuals of each target species were transported to each field
margin at the beginning of the flowering season of OSR crop fields (April
2014). The plants were grouped by species and placed on either side of the
pan trap along the field margin (Fig. 2). The species were 2 m apart, while
plants of the same species were separated by a distance of 1 m. Plants were
watered every four to seven days, depending on the weather conditions. After
six weeks and once the OSR flowering season had concluded, target species
were transported back to the Experimental Fields Service and placed in a
greenhouse that were absent of pollinators. Plants were watered periodically
for two weeks to facilitate the proper development of fruits from the
pollinated flowers. Flower buds were periodically removed to avoid
overestimation of unpollinated flowers. Afterwards, the number of well-
developed fruits and total number of flowers that had not been pollinated
were counted, and these were identified by the scars that were left on the
branches. Fruit set was calculated as the proportion of flowers that set fruit.
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Statistical analyses
The effects of the type of field margin, wildflower resources and density of
non-cropped habitats on the abundance of flower visitors and fruit set were
tested separately for the bees, non-bee flower visitors, and each target
species. The effects of field margin type (OSR-C vs. C-C), wildflower
resources and density of non-cropped habitats on bee and non-bee flower
visitors abundance were analysed with generalized least squares using the
nlme package for R statistical software (Pinheiro et al., 2017). Because some
interactions between the variables were significant, separate models were
used for the different field margins (OSR-C and C-C). OSR flower resources
were included in the OSR-C field margin model to evaluate its effect at field-
level on bee and non-bee flower visitor abundance. The fruit set of each
target species (R. sativus and O. viciifolia) was analysed separately. For each
target species, a generalized linear mixed-effects model with binomial error
distribution was evaluated using the lme4 package in R (Bates et al., 2015).
We separated models by different field margins (OSR-C vs. C-C) when the
interactions between a field margin and another explanatory variable were
significant.
As the bee and non-bee flower visitor data did not meet the
assumptions of normality and constant variance of errors, log transformation
was conducted. Afterward, the abundance of bee and non-bee flower visitor
data was scaled separately by survey. In addition, and to consider the
potential effects caused by the spatial structure of the data, we estimated the
spatial autocorrelation in the residuals of each model by means of the
Moran’s I autocorrelation index, using the spdep package (Bivand and Piras,
2015) an implementation of Legendre’s routines (2000)1 for R. Although
some residual spatial autocorrelation was found for log transformed data, it
disappeared in scaled data; therefore no correction for spatial autocorrelation
was applied to the models. For the fruit set data, no adjustment or correlation
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was needed, since no spatial autocorrelation was detected on original data.
We used the Akaike information criterion (AIC) to select the best model for
each analysis (Akaike, 1973). All statistical analyses were conducted using R
version 3.1.1 (R Core Team, 2016).
1 An R-package implementing these routines to obtain the Moran’s I correlogram is available from J. M. Blanco-Moreno, on request.
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Overview of flower resources and bee and non-bee flower visitors
Overall, 61 and 51 insect-pollinated species in flower were recorded in the
OSR-C and C-C field margins, respectively, during the experimental period
(Table A.1 in Appendix A). We recorded 4242 hymenopterans (15 families,
plus Parasitica and Symphyta specimens), 3500 coleopterans (25 families)
and 23,565 dipterans (40 families) in 21 OSR-C field margins. On 21 study
C-C field margins, we recorded 2682 hymenopterans (15 families, plus
Parasitica and Symphyta specimens), 2796 coleopterans (23 families) and
13,050 dipterans (41 families) (Table A.2 in Appendix A).
Abundance of bee and non-bee flower visitors
Bee abundance was significantly higher in OSR-C than in C-C field margins
(Table 1; p < 0.001). Of the remaining variables examined, only the density
of non-cropped habitats had a significant effect. The density of non-cropped
habitats had a negative effect on bee abundance in the studied field margins
(Table 1; p = 0.006). Multiple significant interactions were found between
the explanatory variables (field margin type, density of non-cropped habitats
and wildflower resources) and the abundance patterns of the non-bee flower
visitors (Table 1). Consequently, we used separate models for each field
margin type (OSR-C and C-C) (Table 2). On the one hand, the abundance of
non-bee flower visitors was significantly affected by the interaction between
OSR flower resources and wildflower resources (Table 2; p = 0.003) in the
OSR-C field margins. Wildflower resources had a significant effect on the
abundance of non-bee flower visitors only at low OSR flower resources
(Fig. 3). On the other hand, the abundance of non-bee flower visitors in the
C-C field margin was increased by wildflower resources when the density of
non-cropped habitats was low (Table 2; Fig. 4). In contrast, the effect of
wildflower resources was negligible when the density of non-cropped
habitats was high (Fig. 4).
RESULTS
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Tab
le 1
. Eff
ect
of f
ield
mar
gin
type
(O
ilsee
d ra
pe-C
erea
l vs
. C
erea
l-C
erea
l),
dens
ity
of l
inea
r fe
atur
es o
f no
n-cr
oppe
d ha
bita
ts
(rad
ius:
500
m)
and
wild
flow
er r
esou
rces
on
the
abun
danc
e of
bee
s (H
ymen
opte
ra:
Apo
idea
) an
d no
n-be
e fl
ower
vis
itors
(H
ymen
opte
ra e
xclu
ding
Apo
idea
, C
oleo
pter
a an
d D
ipte
ra).
Sta
tistic
al s
igni
fica
nce
was
obt
aine
d fr
om t
ype
III
AN
OV
As
with
the
m
inim
um a
dequ
ate
mod
el.
B
ee a
bund
ance
Non
-bee
flow
er v
isito
r ab
unda
nce
E
st
F D
f p-
valu
e E
st
F D
f p-
valu
e F
ield
mar
gin
type
(F
MT
) 0.
90
50.1
4 1
< 0.
001
1.
02
73.5
5 1
< 0.
001
Den
sity
of
non-
crop
ped
habi
tats
(D
nH)
-0.2
9 7.
82
1 0.
006
-0
.33
10.4
3 1
0.00
1 W
ildf
low
er r
esou
rces
(W
fR)
-0.0
3 0.
09
1 0.
764
0.
12
1.79
1
0.18
2 F
MT
× D
nH
0.26
3.
63
1 0.
058
0.
34
6.61
1
0.01
1 F
MT
× W
fR
-0.1
4 1.
24
1 0.
267
-0
.35
8.23
1
0.00
5 D
nH ×
WfR
-0
.06
0.26
1
0.61
2
-0.3
8 10
.07
1 0.
002
FM
T ×
DnH
× W
fR
0.26
2.
72
1 0.
101
0.
39
6.81
1
0.01
0 B
old
valu
es r
epre
sent
sig
nifi
cant
val
ues,
P <
0.0
5.
Tab
le 2
. E
ffec
t of
den
sity
of
linea
r fe
atur
es o
f no
n-cr
oppe
d ha
bita
ts (
radi
us:
500
m),
wild
flow
er r
esou
rces
and
OSR
flo
wer
re
sour
ces
on th
e ab
unda
nce
of n
on-b
ee f
low
er v
isito
rs (
Hym
enop
tera
exc
ludi
ng A
poid
ea, C
oleo
pter
a an
d D
ipte
ra)
for
diff
eren
t fie
ld
mar
gin
type
s (O
ilsee
d ra
pe-C
erea
l vs
. C
erea
l-C
erea
l).
Sta
tistic
al s
igni
fica
nce
was
obt
aine
d fr
om t
ype
III
AN
OV
As
with
the
m
inim
um a
dequ
ate
mod
el.
O
SR-C
fiel
d m
argi
n
C-C
fiel
d m
argi
n
Est
F
Df
p-va
lue
E
st
F D
f p-
valu
e D
ensi
ty o
f no
n-cr
oppe
d ha
bita
ts (
DnH
)
-0.3
3 8.
32
1 0.
005
Wil
dflo
wer
res
ourc
es (
WfR
) -0
.22
10.8
2 1
0.00
1
0.12
1.
43
1 0.
234
OS
R f
low
er r
esou
rces
(O
fR)
-0.0
2 0.
09
1 0.
771
D
nH ×
WfR
-0.3
8 8.
04
1 0.
005
DnH
× O
fR
W
fR ×
OfR
0.
19
9.21
1
0.00
3
DnH
× W
fR ×
OfR
Bol
d va
lues
rep
rese
nt s
igni
fica
nt v
alue
s, P
< 0
.05.
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Fruit set of target species
The fruit set of R. sativus was higher in the OSR-C field margins than in the
C-C field margins (Table 3; p = 0.011). However, the density of non-cropped
habitats and wildflower resources did not significantly affect the fruit set
(Table 3; p = 0.770 and p = 0.685, respectively). The fruit set of O. viciifolia
showed a significant interaction between the field margin type and density of
non-cropped habitats (Table 3; p = 0.042). Therefore, the effects on fruit set
of O. viciifolia were evaluated separately for the OSR-C and C-C field
margins. Fruit set improved according to density of non-cropped habitats and
reduced according to the wildflower resources in the OSR-C field margins
(Table 4; p = 0.015 and p = 0.022, respectively). In the C-C field margins,
the fruit set of O. viciifolia was high under two different scenarios, as shown
by the statistically significant interaction between wildflower resources and
density of non-cropped habitats (Table 4; p = 0.038). Either a high cover of
wildflower resources and a low density of non-cropped habitats or a low
cover of wildflower resources and a high density of non-cropped habitats
increased the fruit set of O. viciifolia in the C-C field margins (Fig. 5).
Table 3. Effect of field margin types (Oilseed rape-Cereal vs. Cereal-Cereal), density of linear features of non-cropped habitats (radius: 500 m) and wildflower resources on the fruit set of target species (Raphanus sativus and Onobrychis viciifolia). Statistical significance was obtained from type III ANOVAs with the minimum adequate model. Bold values represent significant values, P < 0.05.
Raphanus sativus Onobrychis viciifolia
Est χ2 Df p-value Est χ2 Df p-
value Field margin type (FMT) 0.66 6.51 1 0.011 0.36 2.59 1 0.107 Density of non-cropped habitats (DnH)
0.04 0.09 1 0.770 -0.14 0.81 1 0.367
Wildflower resources (WfR) -0.05 0.16 1 0.685 -0.11 0.85 1 0.356 FMT × DnH 0.49 4.14 1 0.042 FMT × WfR DnH × WfR -0.26 3.50 1 0.062 -0.34 5.70 1 0.017 FMT × DnH × WfR
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Figure 3. Effect of wildflower resources (%) and oilseed rape flower resources (%) on non-bee flower visitors abundance (Hymenoptera excluding Apoidea, Coleoptera and Diptera) in oilseed rape-cereal field margins. Lines are generalized least squares model predictions from the model described in Table 2. Note that the log scale is used in the axes.
Figure 4. The effect of wildflower resources (%) and density of non-cropped habitats (km) on the abundance of non-bee flower visitors (Hymenoptera excluding Apoidea, Coleoptera and Diptera) in cereal-cereal field margins. Lines are generalized least squares model predictions from the model described in Table 2. Note that the log scale is used in the axes.
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Table 4. The effect of density of linear features of non-cropped habitats (radius: 500 m) and wildflower resources on fruit set of Onobrychis viciifolia for different field margin types (Oilseed rape-Cereal vs. Cereal-Cereal). Statistical significance was obtained from type III ANOVAs with the minimum adequate model. Bold values represent significant values, P < 0.05. OSR-C field margin C-C field margin
Est χ2 Df p-
value Est χ2 Df
p-value
Density of non-cropped habitats (DnH)
0.15 5.94 1 0.015 -0.22 1.11 1 0.291
Wildflower resources (WfR) -0.15 5.21 1 0.022 -0.21 0.88 1 0.348 DnH × WfR -0.61 4.31 1 0.038
Figure 5. The effect of wildflower resources (%) and density of non-cropped habitats (km) on the fruit set of Onobrychis viciifolia in cereal-cereal field margins. Lines are generalized linear mixed-effects model predictions from the model described in Table 4. Note that the log scale is used in the axes.
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Abundance of bee and non-bee flower visitors
Most studies have shown that the presence of mass flowering crops, such as
oilseed rape, with the support of natural and semi-natural habitats enhances
the abundance of bees (Westphal et al., 2009; Le Féon et al., 2010;
Holzschuh et al., 2013). Our results showed that bee abundance increased in
response to the scattered presence of OSR crops, although the effect of
wildflower resources resulted negligible in highly intensive cereal-dominated
landscapes. OSR crops are an important food resource for bees during the
blooming period (Holzschuh et al., 2011; Westphal et al., 2009). Both honey
bees and wild bees are more abundant nearby mass flowering crops, although
the latter may depend also on the presence of non-crop habitats (Holzschuh
et al., 2011).
The scattered presence of OSR crops also promoted an increased
abundance of non-bee flower visitors. But, the effect of wildflower resources
was only observed when it coincided with a low percentage of OSR flower
resources. Holzschuh et al. (2011, 2016) found a dilution effect of pollinators
related to the expansion of mass flowering crops in the landscape. However,
in our study, the absence of resources provided by OSR flowers and
resource-poor margins promoted the dispersal of non-bee flower visitors to
adjacent areas rich in floral resources. Our results strongly support that
flower visitors abundance has multiple responses depending on the local and
landscape context (Steffan-Dewenter et al., 2002), and these responses can
vary temporally. Nevertheless, our research suggests what may occur in the
short-term, but it cannot indicate what might happen on flower visitor
populations in the long-term.
Our study indicates that changes in landscape structure, as assessed
as the density of non-cropped habitats, affected bee and non-bee flower
visitors differently. The abundance of bees varied in complex, but not in
DISCUSSION
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simple landscapes. Some studies have shown that agricultural areas in
complex landscapes benefit from a spillover effect from adjacent semi-
natural habitats (see Tscharntke et al., 2012). Our results suggest a temporal
concentration of bee populations in the resources provided by OSR fields
principally. On the other hand, landscape structure had a significant effect on
the abundance of non-bee flower visitors when OSR fields were absent. This
landscape effect depends on the abundance of wildflower resources at a local
scale, as shown by the statistically significant interaction between wildflower
resources and density of non-cropped habitats. The local effect of wildflower
resources was positive in a structurally simple landscape, i.e., a low density
of non-cropped habitats, but not in a complex landscape. According to Kleijn
et al. (2011), scarce patches with resources in a poor landscape concentrate
more individuals than numerous patches with resources in a rich landscape.
Our data suggest that non-bee flower visitors are concentrated where
resources are offered by wildflowers in a landscape with a low density of
non-cropped habitats, but not in a landscape with a high density of non-
cropped habitats. In a complex landscape, flower visitors can disperse
throughout the mosaic of non-cropped habitat patches in the landscape. This
response of non-bee flower visitors to the landscape structure should be
considered in conservation management decisions. As such, the preservation
or restoration of wildflower resources in a simple landscape could have a
greater effect on the abundance of non-bee flower visitors than in complex
landscapes (Tscharntke et al., 2012).
Despite the positive effect of mass flowering crops on flower visitor
abundance, particularly on bees, it is necessary to consider their long-term
effects on their populations. Westphal et al. (2009) showed that an increase
of mass flowering crops did not translate into a higher reproductive success
of bumblebee colonies, because resources were limited when the flowering
season finished. In addition, long-term effects on insect populations can be
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related with the inputs of pesticides to the crops. Recent research has
demonstrated the negative effects of pesticides used in mass flowering crops,
for example, on honeybees (Di Prisco et al., 2013) and on bumblebees
(Stanley et al., 2015), and other alternatives may have the same negative
effects on insects (Klatt et al., 2016). Therefore, the benefits offered by mass
flowering crops, in terms of resources, could be diminished by the
continuous pesticide applications.
Fruit set of target species
Mass flowering crops had a positive effect on the fruit set of R. sativus. In
contrast, the fruit set of O. viciifolia was affected by wildflower resources at
a local scale and by the density of non-cropped habitats at landscape scale,
but not by OSR crops. Despite the high attractiveness of mass flowering
crops for pollinators that could enhance the fruit set of R. sativus and O.
viciifolia plants, their contrasting patterns of fruit set reflects strong
differences in their interactions with flower resources at landscape and field
scales. An increase of the fruit set of R. sativus is attributable to a facilitation
process (Rathcke, 1983), as the pollinator visits could be enhanced due to the
presence of the OSR crop. Although a facilitation process can occur between
different floral forms (Ghazoul, 2006), we suggest that the same generalized
open floral structure of OSR and R. sativus may represent an advantage over
O. viciifolia, as its pollination appears to involve more specialized
interactions. In addition to morphological differences, another advantage of
the generalist species is the similitude in flower color with OSR, compared
with the specialist species. Bee visits are more frequent between similar
flowers than between flowers with different colors (Chittka et al., 1999).
Therefore, OSR flower traits combination can increase the pollinator visits
rates to similar flowers (R. sativus) than to dissimilar flowers (O. viciifolia),
affecting their fruit sets. The fruit set of O. viciifolia was enhanced in
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complex landscapes (high density of non-cropped habitats) but diminished
due to wildflower resources of nearby OSR crops. The decrease in fruit set
can be explained by the competition for pollinators between the target
species and species thriving in plant communities in the immediate vicinity
(Rathcke, 1983). For instance, Holzschuh et al. (2011) indicated a decrease
in the seed set of Primula veris L. thriving in grasslands when the percentage
of OSR fields in the landscape increased, suggesting a competition for
pollinators between the study species and crop.
In the vicinity of cereal fields, the fruit set of O. viciifolia increased
with a higher percentage of wildflower resources, especially in a simple
landscape. However, fruit set was enhanced in a complex landscape with a
low percentage of wildflower resources. Since bees do not respond in the
same way as the pollination of O. viciifolia, the effect of the density of non-
cropped habitats in cereal-dominated landscapes suggests that this species
could be pollinated by both bee and non-bee flower visitors. Specialist plant
species, such as O. viciifolia, could be more vulnerable to changes in the
landscape, such as the density of non-cropped habitats, than generalist plant
species, such as R. sativus. In simple landscapes, wildflower resources may
have attracted numerous pollinators that enhance the fruit set of O. viciifolia.
Conversely, the competition process for pollinators occurs between the
wildflower resources and target species in complex landscapes.
These results support our hypothesis that wildflower resources have
different effects on the fruit set of both target species, because generalist and
specialist plant species respond differently to the landscape structure. The
effect of OSR crops and wildflower resources could be beneficial only for
generalist plant species with flowers similar in shape or color to the OSR,
because competition might affect specialist plant species. Further studies that
include direct observation measures of pollinators may help to explain how
the landscape and local factors can affect the flower visitation rates and
define the main service provider in species with different pollination
syndromes.
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Our study suggests that the inclusion of OSR or other mass flowering crops
within crop rotation schemes can promote temporally the increase of the
abundance of bee and non-bee flower visitors. However, the long-term
effects of mass flowering crops on pollinator abundance must be considered
in conservation management decisions. In addition, the management of other
factors, as wildflower resources and density of non-cropped habitats, must
also be considered to improve pollination service in highly intensified
Mediterranean agricultural landscapes.
Fruit set of target plants could not depend exclusively on pollinator
abundance in the landscape, as it appears to also depend on the composition
of the pollinator community. Our results support that plants with different
pollination syndromes may react differently to changes in the environment,
and this is likely to be attributed to the interaction between flower resources
(both crop and wildflower) and the quality of the pollinator community. Our
results highlight the importance of developing agri-environmental schemes
that include OSR crops and maintain wildflower resources in field margins to
improve the pollination services delivered by a diverse ensemble of
pollinators in agricultural landscapes dominated by cereal fields.
Acknowledgements This research was funded by the project “Agricultural intensification, biodiversity and pollination functioning in the Mediterranean region. Development of environmentally friendly farming schemes” (CGL2012-39442) from the Spanish Government, as well as by the FPI-MEC grant (BES-2013-064829) to M. Mendoza-García. We are very grateful to the farmers who allowed us to use their fields and to L. Armengot, P. Baldivieso and several students for their collaboration in the fieldwork. We also thank B. Caballero-López, J. Mederos López from the “Museu de Ciències Naturals de Barcelona” for their help in identifying Diptera.
IMPLICATIONS FOR MANAGEMENT
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Appendix A. Supplementary material Table A.1. The average abundance of wildflower resources present in the six surveys (April to June 2014) for the oilseed rape-cereal and cereal-cereal field margins in Central Catalonia.
Species
Wildflower resources surveys
C-C field margins O-C field margins
1 2 3 4 5 6 1 2 3 4 5 6
Adonis flammea Jacq. 0.2 0.2 1.0
Alyssum alyssoides (L.) L.
1.7
Anacyclus clavatus (Desf.) Pers. 0.3 0.33 20.4 1.3 2.8 1.0 3.1 3.1 3.2 7.1 5.0 5.8
Anthemis arvensis L.
6.8 3.1
6.0 3.7
Astragalus stella L.
0.8
Brassica napus var. oleifera (Moench) DC.
0.3 0.3 0.8 0.3
18 18 15.2 6.9 3.3 0.3
Bryonia dioica Jacq.
0.2 0.2
Calendula arvensis L.
0.2
0.8
8.3 8.3 1.3 1.7 0.8 0.2
Capsella bursa-pastoris (L.) Medik. 0.8 0.8 0.6
0.2
4.5 4.5 1.2 0.8 0.7 0.2
Carduus pycnocephalus L.
1.0 1.0 1.0
6.7 3.3
Carduus tenuiflorus Curtis
0.2 0.2 1.7 3.3 1.7 15.8
Caucalis platycarpos L. 0.2 0.2
0.3 0.3 0.2 0.2
Centaurea cyanus L. 0.2 0.2 0.8 1.0 0.6 1.7
Cerastium glomeratum Thuill.
0.2 0.2
Chaenorhinum minus (L.) Lange
0.2 0.2
Cirsium arvense (L.) Scop.
0.8
0.2
Convolvulus arvensis L.
0.4 0.2
1.0 0.3 0.3
Crepis bursifolia L.
1.67 1.67
Crepis capillaris (L.) Wallr.
0.17
Crepis sancta (L.) Bornm. 0.2 0.2
0.4 0.2
Crepis vesicaria L.
0.2 0.2
Diplotaxis erucoides (L.) DC. 0.4 0.4 0.9 0.9 0.9 0.2 2.2 2.2 3.3 2.1 2.4 2.4
Erodium ciconium (L.) L’Hér. in Aiton 0.3 0.3 2.8 1.8 1.7 1.8 2.4 2.4 4.3 3.8 5.4 3.1
Erodium cicutarium (L.) L’Hér. in Aiton 0.2 0.2
0.5
0.2
0.2 0.2
Erodium malacoides (L.) L’Hér.
0.2
Erucastrum nasturtiifolium (Poir.) O.E. Schulz
0.3
Euphorbia characias L.
2.2
Euphorbia falcata L. 0.3 0.3 0.3 0.3 0.2
0.8
SUPPLEMENTARY MATERIAL
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Euphorbia serrata L. 0.2 0.2
1.7 0.6
0.3 0.3 1.3 0.8 0.8 1.0
Fallopia convolvulus (L.) Á. Löve
1.0 0.3 1.0
Fumaria officinalis L. 2.8 3.1 4.0 2.1 1.7 1.3 3.0 2.9 4.4 2.5 1.0 0.7
Fumaria parviflora Lam.
0.2
Galium aparine subsp. aparine L.
0.2 0.9 0.5
0.2
Galium aparine subsp. spurium (L.) Hartm.
0.3 1.7
Geranium rotundifolium L.
0.7 0.7 1.0 0.9 0.2
Heliotropium europaeum L.
0.2 0.2
Hypecoum imberbe Sm. in Sibth. 0.2 0.2
0.8
1.0 1.0 3.3 2.2 2.3
Hypecoum pendulum L.
0.2 0.2
Hypecoum procubens L.
0.2
0.2 0.2 3.8 2.9 0.2 0.6
Jasminum fruticans L.
0.2 0.2 6.7 6.7 7.5 3.3
Lamium amplexicaule L.
0.8
Lathyrus cicera L. 0.2 0.2 0.8
1.0 0.3
Leontodon taraxacoides (Vill.) Mérat
0.2
Lepidium draba L. 11.7 11.7 5.2 0.9 0.8
5.2 5.2 2.5 0.9 1.0 0.2
Lithospermum arvense L. 1.8 1.8 0.7 0.8 0.8 0.8 0.2 0.2 1.5 1.3 0.7 0.4
Lithospermum fruticosum L.
0.8
Malva sylvestris L.
1.4 2.5 1.7 2.1
0.5 1.4 1.0 1.4
Medicago lupulina L.
0.2 0.2 0.2 0.2
Medicago minima (L.) L.
1.7
Medicago orbicularis (L.) Bartal.
0.5
Medicago polymorpha L. 1.0 1.0 20.0 0.8
0.3 0.2 0.2 0.9
Medicago rigidula (L.) All.
0.2
Medicago sativa L.
0.2 0.8
Medicago truncatula Gaertn.
0.8
Muscari comosum (L.) Mill.
0.2
0.2
Muscari neglectum Guss. ex Ten. 0.2 0.2
0.2 0.2
Onobrychis viciifolia Scop.
0.2
Ononis spinosa L.
1.7
Ornithogalum umbellatum L.
0.2 0.2
Papaver argemone L.
0.2 0.2
5.0 0.6 1.7
Papaver hybridum L.
0.8
Papaver rhoeas L. 1.3 1.3 5.1 3.6 2.6 3.6 0.8 0.8 5.1 9.6 6.4 7.0
Polygonum aviculare L.
1.8 1.8 0.3 1.7 1.7 2.5
Reseda phyteuma L.
0.2
0.2 0.2 0.2 0.2 0.2 0.8
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Salvia verbenaca L. 10.0 10.0 0.8 1.7 1.7 3.3
Scandix pecten-veneris L. 3.3 3.3 3.3 0.6 0.8
3.0 3.0 6.0 0.6 0.8
Senecio vulgaris L. 0.2 0.2
0.2 0.2 0.4 0.4 0.2 0.2
Silene vulgaris (Moench) Garcke
0.5 0.7
Silybum marianum (L.) Gaertn.
0.3 1.0 0.2
0.3 0.2
Sisymbrium officinale (L.) Scop.
0.8 0.8
Solanum nigrum L.
0.2
Sonchus oleraceus L.
0.8
0.8 0.8
0.2
Sonchus tenerrimus L.
0.2
0.3
Taraxacum officinale Weber in Wiggers
0.2 0.2
Torilis nodosa (L.) Gaertn.
0.2 0.2
Veronica hederifolia L. 0.2 0.2
Veronica pérsica Poir. in Lam.
0.8
Vicia peregrina L. 0.5 0.5 1.8 0.9 0.8
0.8 0.2 2.5
Vicia sativa L.
1.3 3.3 0.2
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Table A.2. Total non-bee flower visitor (Hymenoptera excluding Apoidea, Coleoptera and Diptera) and bee (Hymenoptera: Apoidea) abundance collected by pan traps during the six surveys (April to June 2014) in the oilseed rape-cereal and cereal-cereal field margins in Central Catalonia.
Crop Order Flower visitor surveys
1 2 3 4 5 6
OSR
Coleoptera 276 631 1,450 311 281 551 Diptera 2,207 4,194 9,115 5,031 1,500 1,518
Hymenoptera (excluding Apoidea)
83 202 500 487 387 418
Bees 108 312 448 693 306 440
Cereal
Coleoptera 122 246 1,268 285 417 458
Diptera 1,771 2,661 4,718 1,980 842 1,078 Hymenoptera (excluding Apoidea)
55 115 393 316 362 228
Bees 28 169 433 241 165 247
Total 4,650 8,530 18,325 9,344 4,260 4,938 50,047
179
El estudio de los efectos de la intensificación agrícola sobre la biodiversidad
ha adquirido una gran relevancia en la literatura científica en los últimos
años. En este contexto, muchos estudios han evaluado las consecuencias
generadas por dicha intensificación sobre los visitantes florales, en particular,
sobre las abejas (apoideos). Sin embargo, el conocimiento acerca de los
efectos sobre otros visitantes florales, como coleópteros y dípteros, es mucho
menor. Asimismo, muchos de estos estudios han inferido, a partir de los
resultados obtenidos en los visitantes florales o por su interacción con las
plantas, las posibles consecuencias en la polinización. No obstante, la
evaluación directa de la polinización, a través de medidas como la
producción de frutos, proporciona un enfoque más preciso de los efectos de
la intensificación agrícola sobre este servicio ecosistémico. En este estudio se
evalúan los efectos de la intensificación agrícola, a diferentes niveles, sobre
la abundancia y composición de los principales grupos de visitantes florales,
que incluyen apoideos, coleópteros y dípteros. También se evalúan los
efectos sobre la producción de frutos en dos especies diana con diferente
grado de especialización en su interacción con los visitantes florales
(generalista y especialista). A continuación, se detallan los principales
resultados obtenidos, así como también las implicaciones para la gestión de
dichos paisajes agrícolas.
Diversos estudios han demostrado que la reducción del área dedicada
al uso agrícola favorece el incremento de los visitantes florales en el paisaje
(Bommarco et al., 2010; Westphal et al., 2008; Winfree, Aguilar, Vázquez,
LeBuhn, & Aizen, 2009). Esto coincide con los resultados encontrados en
nuestro estudio, en donde el gradiente de intensificación agrícola a nivel de
paisaje (PAL) afectó la abundancia de los visitantes florales, debido a las
diferencias en la intensidad del uso de la tierra (Capítulo 1). El PAL también
afectó la composición de los visitantes florales, pero independientemente de
DISCUSIÓN GENERAL
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la posición en el campo (Capítulo 3). El paisaje es un importante moderador
de la respuesta de los visitantes florales a la intensidad de la gestión (Batáry
et al., 2011). En este sentido, la disponibilidad de los recursos requeridos por
los visitantes florales, como por ejemplo las fuentes de alimentación y los
hábitats para la anidación, puede ser modificada por la estructura del paisaje
(Kremen et al., 2007). Además, diversos estudios han demostrado que la
intensificación agrícola ha generado cambios en la composición de la
comunidad de los visitantes florales (Andersson, Birkhofer, Rundlöf, &
Smith, 2013; Cole et al., 2002). Nuestros resultados indican que la
comunidad de visitantes florales fue afectada por los cambios acontecidos a
nivel de paisaje, en relación con la intensificación agrícola.
Asimismo, la intensificación a nivel de paisaje se correlaciona con
cambios en la composición florística de las comunidades vegetales de los
márgenes de los campos y de algunos atributos florales de la comunidad
("community-weighted mean", CWM). Dos de los atributos que cambiaron
en relación con el PAL estaban relacionados con la atracción de los visitantes
florales (tamaño y color de la flor), y el tercero de los atributos está
relacionado con la temporalidad de la disponibilidad de recursos (inicio de la
floración). En cambio, en el centro de los campos, la composición
taxonómica de los ensamblajes de especies y el CWM de sus atributos
florales respondieron, en gran medida, a las prácticas agrícolas a nivel de
campo (Capítulo 3). Estos resultados coinciden con otros estudios donde se
muestra que la composición y algunos atributos de las especies que colonizan
el centro del campo (p. ej. área específica foliar, forma de vida), varían en
relación con la intensificación agrícola a nivel de campo (Guerrero et al.,
2014; José-María et al., 2011). Una de las principales causas de los cambios
provocados en el centro del campo se atribuye a las periódicas
perturbaciones del suelo, como consecuencia de la intensidad de la gestión
de las prácticas agrícolas. Por el contrario, la composición de las
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comunidades que habitan en el margen del campo varía principalmente en
relación con la simplificación del paisaje circundante (Solé-Senan et al.,
2014). Nuestros resultados sugieren que las prácticas agrícolas deben ser
consideradas en el mantenimiento de las comunidades vegetales,
especialmente de aquellas localizadas en el centro de los campos.
Los efectos del PAL también se evidenciaron en la producción de
frutos de las especies diana (Capítulo 1). Por ejemplo, el incremento del PAL
afectó negativamente la producción de frutos de la especie de polinización
generalista estudiada (Raphanus sativus), lo cual coincidió con la reducción
de los visitantes florales, relacionado con la reducción de la superficie
ocupada por hábitats seminaturales y naturales en el paisaje. Otros estudios
han demostrado el efecto negativo en la producción de semillas y de frutos
de especies generalistas al incrementar la distancia a dichos hábitats
(Albrecht et al., 2007; Steffan-Dewenter & Tscharntke, 1999). Este patrón
puede estar relacionado con la abundancia de los visitantes florales en el
paisaje. Aunque los resultados presentados en el Capítulo 1 demostraron que
el incremento del PAL se correlacionó positivamente con la abundancia de
abejas y coleópteros (ver Morrison, Izquierdo, Plaza, & González-Andújar,
2017), mientras que los dípteros no se beneficiaron del aumento del PAL.
Por ende, es importante considerar el conjunto total de visitantes florales que
contribuyen a los servicios de polinización en los paisajes agrícolas.
Efectos de la agricultura ecológica a nivel de paisaje y de parcela
Además de analizar las consecuencias generadas por la intensificación
agrícola (PAL) sobre los visitantes florales y sobre la polinización, también
es necesario evaluar los efectos de la implementación de los diversos
esquemas agroambientales, como es la agricultura ecológica. Los efectos de
este esquema sobre la abundancia y diversidad de visitantes florales han sido
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evaluados en múltiples estudios (Holzschuh et al., 2008; Purtauf et al., 2005;
Rundlöf et al., 2008). Sin embargo, pocos estudios se han enfocado en la
evaluación directa de la polinización, como es la producción de frutos. En
concreto, en este estudio se evaluaron los efectos de la agricultura ecológica
a nivel de paisaje (Capítulo 2) y de campo (Capítulo 1, 2 y 3), tanto en la
abundancia y composición de los visitantes florales, como en la producción
de frutos de especies diana.
A nivel de paisaje, la proporción de tierra arable bajo gestión
ecológica (POL, por sus siglas en inglés) no incrementó la abundancia de las
abejas, lo cual coincidió con otros estudios (Brittain et al., 2010; Happe
et al., 2018). La abundancia de abejas puede ser favorecida por el incremento
del uso agrícola en el paisaje (Capítulo 1), siendo mayor este efecto que el
causado por la gestión a nivel de campo. En contraste, Holzschuh et al.
(2008) mostró que un incremento en la proporción de cultivos ecológicos
aumentó la riqueza y densidad de abejas. Este aumento fue promovido
principalmente por las diferencias en la cobertura de recursos florales entre
los campos orgánicos y convencionales, tanto en el margen del campo como
en el cultivo. Es decir, las abejas podrían concentrar su actividad únicamente
en aquellos parches que provean la mayor cantidad de recursos florales. En
este sentido, en nuestro estudio el aumento de la POL no proporcionó las
condiciones necesarias para incrementar la abundancia de dichos visitantes
florales, por lo que otros factores como el PAL marcaron principalmente la
respuesta de los visitantes florales.
En referencia al efecto de la POL sobre la producción de frutos de las
plantas diana, este fue diferente dependiendo de su grado de especialización
en la polinización de la planta diana (Capítulo 2). Los resultados indicaron
que la POL únicamente incrementó la producción de frutos de la especie de
polinización generalista (R. sativus). Esto coincide con otros estudios que
muestran un efecto positivo de la agricultura ecológica en los servicios de
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polinización, en particular, sobre la producción de frutos de especies con una
estructura floral abierta (Hardman et al., 2016; Power & Stout, 2011).
Considerando que la POL no tuvo un efecto sobre la abundancia de abejas,
las cuales son los principales visitantes florales de la especie especialista
(Onobrychis viciifolia), el aumento de la producción de frutos de la especie
de polinización generalista pudo estar mediado por la actividad de otros tipos
de visitantes florales. Esto concuerda con los resultados presentados en los
Capítulos 1 y 4, donde se muestra un incremento del éxito de la producción
de frutos en las plantas diana que correlaciona positivamente con la
abundancia de otros visitantes florales (coleópteros, dípteros y otros
himenópteros), lo que nos permite hipotetizar que estos otros grupos de
visitantes florales también pueden contribuir en los servicios de polinización
en los paisajes agrícolas (Rader et al., 2016).
Por otra parte, la intensidad de la gestión (ecológica vs.
convencional), el tipo de cultivo (cereal vs. leguminosa) y los recursos
florales a nivel de parcela, también afectaron a los visitantes florales y a la
polinización. Los campos ecológicos tuvieron un efecto positivo sobre los
visitantes florales, independientemente del paisaje circundante (Capítulo 1).
Sin embargo, este efecto positivo estuvo limitado al centro de los campos de
cereales. En este sentido, los resultados sugieren un efecto restringido de la
gestión ecológica a nivel de parcela, que no se extiende sobre los márgenes
ni sobre el paisaje en que se encuentran inmersos los campos con dicha
gestión. Por otro lado, los cultivos de leguminosas, aunque tuvieron un
efecto positivo, fue menos pronunciado, y sólo algo más acusado sobre los
coleópteros florícolas. El aumento de aquellos visitantes menos
especializados parece relacionarse con una mayor disponibilidad de recursos
florales en el paisaje. Sin embargo, en la evaluación realizada en el
Capítulo 2, los recursos florales ubicados en el margen del campo no
incrementaron la abundancia de las abejas, independientemente de la
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intensidad de la gestión del campo colindante. De igual forma, los campos de
leguminosas no tuvieron un efecto sobre la abundancia de las abejas en los
márgenes colindantes. Se ha demostrado que una alta abundancia de recursos
en el paisaje, como la que constituye la floración de los campos de
leguminosas, puede producir la dilución de los visitantes florales (Veddeler,
Klein, & Tscharntke, 2006).
En los paisajes agrícolas, además de considerar el efecto de la
abundancia de los recursos florales sobre los visitantes florales, también es
necesario evaluar el efecto de la composición y el CWM de sus atributos
florales sobre la composición de los visitantes florales. Los resultados
presentados en el Capítulo 3 mostraron que la composición de la comunidad
vegetal ubicada en el margen del campo influyó en la composición de los
visitantes florales. Sin embargo, la composición de la comunidad vegetal
localizadas en el centro del campo no explicó la composición de los
visitantes florales. Estos resultados pueden estar relacionados con la baja
abundancia de plantas y visitantes florales encontradas en el centro del
campo, comparada con la encontrada en el margen (Capítulo 1). Este estudio
sugiere que la simplificación del paisaje puede tener un efecto indirecto en la
composición de los visitantes florales, a través de los cambios que se generan
en la composición de recursos florales en los márgenes de los campos.
El CWM de los atributos florales influyó en la composición de la
comunidad de visitantes florales, tanto en el centro como en el margen del
campo (Capítulo 3). Es importante tener en cuenta que la respuesta de los
grupos de visitantes florales (apoideos, coleópteros y dípteros) al CWM de
los atributos florales fue diferente entre ellos. La preferencia de los insectos a
visitar un tipo específico de flor depende del diseño floral, por ejemplo del
color y el tamaño de la flor, de las recompensas florales y de la disposición
de las flores en la inflorescencia (Goulson, 1999). Sin embargo, dicha
elección también puede depender de múltiples atributos florales (Hegland &
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Totland, 2005). En este estudio (Capítulo 3), se mostró que la respuesta de
los visitantes florales a determinados atributos florales se mantuvo constante,
a pesar de que la composición de las comunidades vegetales y de visitantes
florales varió entre ambos años de muestreo (2013 y 2015). Por ejemplo, el
color de la flor afectó la composición de los visitantes florales en el margen
del campo, mientras que el tamaño de la flor influyó dicha composición en el
centro del campo. Las preferencias de los visitantes florales por los colores
de la flores no correspondieron con los expuestos en los síndromes clásicos
de polinización (Faegri & Van Der Pijl, 1979). A pesar de ello, los resultados
mostraron un patrón de importancia biológica, en el que las familias de los
diferentes grupos de visitantes florales respondieron de forma similar a los
mismos colores en ambos años de muestreo. No obstante, en otros estudios
llevado a cabo en pastizales y matorrales mediterráneos no se encontró una
relación entre los colores de la flor y la composición de los visitantes florales
(Bosch et al., 1997; Reverté, Retana, Gómez, & Bosch, 2016).
La comunidad de visitantes florales, en particular los coleópteros y
los dípteros, no solo respondieron al color de la flor, sino también a la
fenología de los ensamblajes de la comunidad vegetal en el segundo año de
muestreo (Capítulo 3). Esta respuesta pudo estar asociada al incremento de
intensificación en el paisaje, que según Guerrero et al. (2014), promueve una
floración más temprana de las comunidades vegetales, con el fin de evitar la
competencia con los cultivos. En este sentido, la comunidad de visitantes
florales pudo responder a este patrón a través del incremento de aquellas
especies que se ven atraídas por las especies de fenología más temprana. Los
resultados de este estudio también mostraron que la composición de los
dípteros respondió al tamaño de la flor de las plantas en el centro del campo.
Algunos estudios han demostrado que los visitantes florales pueden
discriminar entre flores, basándose en el tamaño de la flor (Elle & Carney,
2003; Kennedy & Elle, 2008). Esta preferencia de los visitantes florales
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puede estar causada por la correlación positiva que hay entre el ancho de la
corola y las recompensas florales (Kennedy & Elle, 2008). Además, los
recursos florales que se encontraban en el centro del campo estaban rodeados
por el cultivo (cereal), por lo que las flores de mayor tamaño pueden
incrementar su visibilidad para los visitantes florales, los cuales concentran
su actividad en los márgenes de los campos (Capítulo 1).
Las repercusiones, directas e indirectas, que estas variables
ambientales tienen sobre la producción de frutos son variables, pues
dependen tanto de las características de la planta que es polinizada como de
las características del entorno inmediato de esta. En el Capítulo 1, donde se
evaluó el efecto del incremento de PAL, no se encontraron diferencias en la
producción de frutos de la especie de polinización generalista en el centro o
en el margen de los campos con una alta intensidad de gestión. Sin embargo,
los recursos florales favorecieron la producción de frutos de la especie diana.
Por ejemplo, en los campos de cultivos de leguminosas, la producción de
frutos no dependió de las condiciones del paisaje. Por el contrario, los
recursos locales localizados en los márgenes y los bordes de los campos
afectaron negativamente la producción de frutos, tanto de la especie
generalista (R. sativus) como especialista (O. viciifolia) (Capítulo 2).
La comunidad vegetal puede afectar los servicios de polinización, por
ejemplo, a través de la competencia por los polinizadores (Kremen et al.,
2007; Pleasants, 1981). Sin embargo, la gestión ecológica y los cultivos de
leguminosas afectaron positivamente la producción de frutos de ambas
especies, siendo mayor el efecto sobre la especie especialista. En algunos
casos, puede ocurrir el proceso de facilitación entre especies con formas
florales similares (Ghazoul, 2006), y ambas pueden beneficiarse de la
concentración de los visitantes florales. Nuestros resultados sugieren que el
incremento en la producción de frutos fue mayor en la especie especialista
debido a la similitud con las flores de los cultivos de leguminosa, ya que
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también pertenece a la familia Leguminosae. Por lo tanto, la disponibilidad
temporal de los recursos ofrecidos por los cultivos de leguminosa puede
afectar la producción de frutos de las especies.
Efecto de los cultivos de floración masiva
Otra de las medidas a considerar en los paisajes agrícolas son los cultivos de
floración masiva. En la evaluación realizada en el Capítulo 4, se encontró
que la presencia de cultivos de colza dispersos en el paisaje incrementó la
abundancia de las abejas (apoideos), así como la de otros visitantes florales
(otros himenópteros, coleópteros y dípteros). Diversos estudios han mostrado
que la presencia de cultivos de floración masiva, en conjunción con los
hábitats naturales y seminaturales, incrementan la abundancia de las abejas
(Holzschuh et al., 2013; Le Féon et al., 2010; Westphal et al., 2009). No
obstante, nuestro estudio indica que los recursos florales de especies no
cultivadas no tuvieron un efecto significativo sobre la abundancia de las
abejas, y solo incrementaron la abundancia de otros visitantes florales
cuando coincidieron con un bajo porcentaje de los recursos ofrecidos por el
cultivo de colza. Por otro lado, algunos estudios han encontrado que la
expansión de los cultivos de floración masiva pueden causar la dispersión de
los polinizadores en el paisaje (Holzschuh, Dormann, Tscharntke, & Steffan-
Dewenter, 2011; Holzschuh et al., 2016). Sin embargo, en los paisajes
agrícolas mediterráneos con márgenes muy pobres en recursos florales,
cuando los cultivos de colza ya no están en flor, se genera la dispersión de
los visitantes florales. Estos resultados sugieren que la respuesta de la
abundancia de los visitantes florales depende del contexto a nivel local y de
paisaje.
Aunado al efecto de los cultivos de floración masiva, la estructura del
paisaje (densidad de márgenes) también afectó la abundancia de las abejas y
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la de otros visitantes florales. La abundancia de abejas incrementó en los
paisajes complejos, pero no en los simples. Se ha demostrado que las áreas
agrícolas localizadas en paisajes complejos se benefician, a través del efecto
de “spillover”, de las áreas naturales y seminaturales adyacentes (Tscharntke
et al., 2012). En este sentido, nuestros resultados sugieren que la
concentración temporal de la población de abejas se debe principalmente a
los recursos ofrecidos por los cultivos de colza (Capítulo 4). Por otro lado, la
estructura del paisaje afectó la abundancia de otros visitantes florales cuando
el período de floración de los cultivos de colza había finalizado y, por tanto,
cesó la disponibilidad de los recursos ofrecidos por el cultivo. En
consecuencia, el efecto del paisaje dependió de la abundancia de los recursos
florales a nivel local. Además, el efecto de estos recursos fue positivo en los
paisajes simples (con una baja densidad de márgenes), pero no en los
paisajes complejos (con una alta densidad de márgenes). Por lo tanto, es
posible que estos otros visitantes florales se concentraran en las áreas con
recursos florales ofrecidos por las plantas arvenses en paisajes con una baja
densidad de márgenes, pero no en paisajes con una alta densidad. En estos
paisajes complejos, en cambio, es factible que los visitantes florales se
dispersaran en los hábitats que no estaban cultivados. Por estas razones, la
estructura del paisaje debe ser considerada en la toma de decisiones de
conservación y manejo, especialmente, para otros visitantes florales.
En relación con el efecto de los cultivos de floración masiva sobre la
producción de frutos, se encontró un efecto positivo sobre la especie de
polinización generalista (R. sativus). Por el contrario, la especie de
polinización especialista (O. viciifolia) fue afectada por los recursos florales
a nivel local y por la estructura del paisaje, sin embargo no por los cultivos
de colza. Estos resultados reflejan importantes diferencias en la interacción
de las especies diana con los recursos florales a nivel de parcela y de paisaje.
Por una parte, el incremento en la producción de frutos de la especie de
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polinización generalista puede ser atribuido al proceso de facilitación
(Rathcke, 1983), donde el incremento de las visitas de polinizadores (y en
consecuencia de producción de frutos) se debe a la presencia de los cultivos
de colza. Además de ello, la flor de la especie de polinización generalista
presenta características similares a la del cultivo de colza (estructura floral
abierta y colores similares), lo que pudo representar una ventaja sobre la
especie de polinización especialista. Por lo tanto, la combinación de
determinados atributos en las flores de colza pudo incrementar las visitas de
los polinizadores en flores similares, como la de R. sativus. Por otra parte, la
producción de frutos de la especie de polinización especialista incrementó en
paisajes complejos, pero disminuyó debido a los recursos florales cerca de
los cultivos de colza. Esta disminución puede atribuirse a la competencia por
los polinizadores entre la especie de polinización especialista y la comunidad
vegetal adyacente (Rathcke, 1983). En general, la especies especialistas son
más vulnerables a los cambios en el paisaje que las especies generalistas
(Biesmeijer et al., 2006). La producción de frutos de la especie de
polinización especialista incrementó cuando aumentó la abundancia de los
recursos florales cerca de los cultivos de cereal, especialmente en los paisajes
simples. En los paisajes complejos, la producción de frutos incrementó
cuando coincidió con un bajo porcentaje de recursos florales. Debido a que
las abejas no respondieron de forma similar a la especie de polinización
especialista, el efecto causado por la densidad de márgenes sugiere, a pesar
de la especialización asumida, que esta especie pudo ser polinizada por otros
visitantes florales, además de las abejas.. En los paisajes más simplificados,
los recursos florales pudieron atraer numerosos visitantes florales que
incrementaron la producción de frutos de la especie de polinización
especialista. En contraste, en los paisajes complejos los recursos florales y la
especie diana pudieron competir por los visitantes florales. En este sentido,
las medidas orientadas a preservar los servicios ecosistémicos de
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polinización deben considerar tanto el nivel de parcela como el de paisaje
para garantizar el éxito reproductivo de especies con diferentes grados de
especialización en su polinización en los paisajes agrícolas.
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La tesis doctoral estudia el efecto de la intensificación agrícola a nivel de
paisaje y de parcela sobre el funcionamiento de la polinización en los
paisajes agrícolas mediterráneos dominados por los cultivos herbáceos
extensivos, mediante el análisis de la abundancia y composición de los
principales grupos de visitantes florales y la producción de frutos de especies
diana con diferentes síndromes de polinización (generalista vs. especialista).
A continuación, se enumeran las principales conclusiones:
1. La intensificación agrícola a nivel de paisaje afecta negativamente la
abundancia de los visitantes florales, sin embargo, en la región de
estudio este patrón se debe fundamentalmente a la respuesta de los
dípteros, mientras que apoideos y coleópteros responden positivamente
la a intensificación a nivel de paisaje.
2. La gestión ecológica a escala de parcela tiene un efecto positivo sobre la
abundancia total de los visitantes florales. Estos efectos solo son
importantes en el centro de los campos, y su relevancia es menor en los
paisajes complejos y en los márgenes de los campos. Sin embargo, para
los apoideos, que son consideradas los polinizadores más efectivos, los
efectos de la gestión ecológica no se manifiestan a nivel de paisaje, ya
que la proporción de tierra arable bajo gestión ecológica no incrementa
su abundancia.
3. Cuando se considera la variación de los recursos florales a diferentes
niveles, su incremento tiene un efecto positivo sobre la abundancia de
todos los grupos de visitantes florales. Sin embargo, el incremento de
dichos recursos en el centro de los campos, debido a los cultivos de
leguminosas, solo promueve la abundancia de los visitantes florales
pertenecientes al grupo de los coleópteros.
CONCLUSIONES
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4. En paisajes con una alta proporción de tierra arable bajo gestión
ecológica, los recursos florales localizados en los márgenes de los
campos no generan un incremento de la abundancia de los apoideos. Por
el contrario, los recursos ofrecidos por los cultivos de leguminosas
causan una reducción de su abundancia en los márgenes.
5. Los cultivos de floración masiva y los recursos florales a nivel de
parcela tienen diferentes efectos sobre la abundancia de apoideos y
sobre la abundancia de otros visitantes florales. Los cultivos de colza
incrementan la abundancia de apoideos, aunque esta disminuye en los
paisajes complejos con más densidad de márgenes. La abundancia de
otros visitantes florales depende de la estructura del paisaje; ya que se
concentran en los recursos florales disponibles en los paisajes simples,
pero no en los paisajes complejos.
6. Las respuestas de los visitantes florales a las características del paisaje, a
la gestión y a la disponibilidad de recursos florales no se manifiestan de
forma directa en cambios en la producción de frutos de plantas diana
(fitómetros); por esta razón, es importante considerar simultáneamente
los efectos sobre los visitantes florales y sobre los servicios que proveen,
preferentemente sobre especies con grados de especialización en la
polinización diferenciados.
7. La intensificación agrícola a nivel de paisaje afecta negativamente la
producción de frutos de la planta de polinización generalista, pero esta
es beneficiada mediante el incremento de los recursos florales a nivel de
parcela.
8. La proporción de tierra arable bajo gestión ecológica a nivel de paisaje
incrementa la producción de frutos de la especie de polinización
generalista, pero no tiene un efecto sobre la especie de polinización
193
especialista. La producción de frutos de ambas especies puede
incrementar debido a la disponibilidad de recursos florales a nivel de
campo que concentra los visitantes florales en determinadas zonas del
paisaje agrícola, pero también puede disminuir debido a la competencia
con la oferta floral localizada en las inmediaciones.
9. Los cultivos de floración masiva tienen un efecto positivo sobre la
producción de frutos de la especie de polinización generalista; por el
contrario, los recursos florales a nivel de parcela y la estructura del
paisaje afectan la producción de frutos de la especie de polinización
especialista.
10. La intensificación agrícola, la intensidad de gestión, el tipo de cultivo y
la distancia al margen del campo afectan la composición de la
comunidad vegetal y sus atributos florales, mientras que la composición
de familias de visitantes florales responde a la intensificación agrícola a
nivel de paisaje.
11. Los atributos florales de la comunidad vegetal influencian la
composición de familias de los visitantes florales; el color y el inicio de
la floración afectan la composición en el margen del campo, mientras
que el tamaño de la flor influencia la composición en el centro del
campo.
194
Implicaciones para la gestión y el desarrollo de medidas
agroambientales
Los resultados obtenidos en los diferentes estudios constituyen una base para
la implementación de medidas agroambientales a diferentes niveles, tanto de
paisaje como de parcela, con el objetivo de armonizar la producción de los
cultivos con el mantenimiento de los servicios ecosistémicos, como la
polinización, en los paisajes cerealistas mediterráneos.
La mejora del servicio de la polinización en los paisajes agrícolas,
mediado por la comunidad de visitantes florales, requiere la aplicación de
medidas que consideren tanto la abundancia como la composición de esta
comunidad. A pesar de que el incremento de la proporción de tierra arable
bajo gestión ecológica parece no incrementar la abundancia de las abejas en
los paisajes agrícolas estudiados, otros visitantes florales pueden beneficiarse
de dichas condiciones. Además, las medidas agroambientales para promover
la abundancia de los visitantes florales deberían evitar la simplificación del
paisaje, mediante la conservación elementos de vegetación natural o
seminatural, como son los márgenes de los campos, así como la
implementación de la agricultura ecológica. Estos cambios tienen relación de
manera directa, por una parte, con la estructura del paisaje agrícola, pero por
otra parte con los efectos causados por su relación con la comunidad vegetal
presente en estos sistemas agrícolas. Estas medidas, no solo pueden
incrementar la abundancia de visitantes florales, sino que también pueden
afectar a la composición de la comunidad, ya que las respuestas de los
diferentes grupos de visitantes florales a los atributos florales de las
comunidades vegetales no son uniformes. Por lo tanto, se recomienda la
selección previa de las especies vegetales, basada en sus atributos florales,
para establecer en los márgenes de los campos, con la finalidad de facilitar la
presencia de visitantes florales específicos, lo cual a su vez sustentará el
servicio de la polinización. En este contexto, este estudio también sugiere
que puede ser beneficiosa la inclusión de cultivos que ofrezcan recursos
195
florales, como las leguminosas, e incluso de floración masiva, como por
ejemplo de colza, dentro de los esquemas de rotación de cultivos. Esta
medida puede promover el incremento temporal de la abundancia tanto de
abejas como de otros visitantes florales.
Debido a que la intensificación agrícola también comporta cambios
en la composición de las comunidades vegetales que habitan en los márgenes
de los cultivos, se deben aplicar diversas medidas agroambientales, aunque a
un nivel diferente del considerado para los visitantes florales. Este estudio
sugiere que la gestión a nivel de parcela y, en particular, la implementación
de prácticas agrícolas de baja intensidad como la agricultura ecológica,
puede ser una medida adecuada, ya que sus efectos sobre la comunidad
vegetal son los de mayor intensidad.
A pesar de que la simplificación del paisaje, bajo los condicionantes
sociales y económicos actuales, es difícilmente reversible, su efecto negativo
sobre la producción de frutos se puede aminorar mediante el incremento de
la disponibilidad de recursos florales en los márgenes. Los beneficios
derivados de este incremento, de acuerdo con nuestros estudios, parecen
tener un carácter amplio y favorecerían especialmente las especies de
polinización generalista. De igual forma, el incremento de la proporción de
tierra arable bajo gestión ecológica a nivel de paisaje también beneficiaría
especies de polinización generalista. Sin embargo, este estudio señala que la
inclusión de cultivos de leguminosa, además de procurar servicios
agronómicos como la fijación de nitrógeno, también pueden ofrecer
temporalmente abundantes recursos florales que benefician la producción de
frutos de las plantas entomófilas, independientemente del síndrome de
polinización de la planta. En este sentido, incluir cultivos de floración masiva
así como mantener los recursos florales de los márgenes de los campos,
puede optimizar el servicio de polinización, procurado por un amplio y
diverso conjunto de visitantes florales en los hábitats agrícolas de los paisajes
mediterráneos.
196
The doctoral thesis studies the effects of agricultural intensification at the
landscape and at the field level on the pollination in Mediterranean
agricultural landscapes dominated by extensive arable crops, through the
analysis of the abundance and composition of the main groups of flower
visitor insects and the fruit set of target species with different degree of
pollination specialization (generalist vs. specialist). Below are presented the
main conclusions:
1. Agricultural intensification at landscape level affects negatively the
abundance of flower-visiting insects; however, in the studied region this
pattern is mainly related to the response of Diptera, whereas Apoidea
and Coleoptera respond positively to landscape level intensification.
2. Organic farming management applied at field level has a positive effect
on the overall abundance of flower visitors, but its effects are only
important in field centres, and of lesser importance in complex
landscapes and in field margins. However, for bees, which are the most
effective pollinators, the effects of organic farming do not scale up at
landscape level, because the proportion of organically managed arable
land does not enhance their abundance.
3. When the variation of flower resources over the landscape is considered,
increasing flower resources have a positive effect on the abundance of
all flower visitor groups. Nonetheless, the increase of flower resources
in field centres by sown legumes is only relevant for the abundance of
Coleoptera flower visitors.
4. Nevertheless, in landscapes with a high proportion of organically
managed arable land, the abundance of bees is not enhanced by the
CONCLUSIONS
197
wildflower resources in the field margins, and the flower resources
offered by legume crops promote a dilution of bees in the field margins.
5. Bee and non-bee flower visitors are affected by different factors in
intensively managed landscapes where mass flowering crops are
present. Bee abundance is enhanced by oilseed rape crops, but their
abundance decreases in complex landscapes with higher density of field
margins. The abundance of non-bee flower visitors depends on the
landscape structure; they are concentrated where resources are offered
by wildflowers in simple landscapes, but not in complex landscapes.
6. The responses of flower visitors to the landscape, management and
availability of flower resources do not translate directly into differences
in the fruit set of phytometer plants; therefore, it is important to consider
simultaneously the effects of on the flower visitors and on the service
they deliver, preferably on plants with differing level of pollination
specialization.
7. The increase of agricultural intensification at landscape level has a
negative effect on the fruit set of plant species of generalist pollination,
but it is benefited through the increase of availability of flower resources
at field level.
8. The proportion of organically managed land enhances the fruit set of
species of generalist pollination, whereas it does not have an effect on
species of specialist pollination. At field level, increasing local
availability of flower resources can enhance the delivery of pollination
services, whereas in the immediate vicinity to target plants it can
actually decrease the fruit set.
9. Mass flowering crops have a positive effect on the fruit set of species of
generalist pollination in the immediate vicinity, whereas the fruit set of
198
plant species of specialist pollination is affected by wildflower resources
at a local scale and landscape structure.
10. Plant species composition and the community-weighted mean of flower
traits in the field margin and field centre varied in relation to
intensification at landscape level, and intensity of farming, crop type and
position within fields at field level. However, flower visitor composition
both in field margins and centres only responds to intensification at
landscape level.
11. The community-weighted means of wildflower resources' traits
influence the community of flower visitors. The flower colour and
flowering onset affect the flower visitor composition in the field
margins, whereas the flower size is the main driver of composition in
field centres.
199
Management implications and development of agri-environmental
measures
The results of our different studies provide the grounds for the
implementation of agro-environmental measures at different levels,
regarding both landscape and field, with the aim of harmonizing the fruit set
with the maintenance of ecosystem services, such as pollination, in
Mediterranean landscapes.
The improvement of pollination services in agricultural landscapes,
which is mediated by the flower visitor community, requires the application
of strategies that consider both the abundance and the composition of this
community. Although an increment in the proportion of organically managed
arable land did not enhance the abundance of bees in the agricultural
landscapes under study, other flower visitors could also benefit from these
conditions. Moreover, agri-environmental measures to promote the
abundance of flower visitors should avoid simplifying the landscape, through
the preservation of natural or semi-natural vegetation elements, like field
margins, and should implement organic farming. The changes are directly
related to the structure of the agricultural landscape, as well as with the
effects caused by the relationship with the existing plant community. These
measures can increase the abundance of flower visitors and they can also
affect the community composition, because the responses of different groups
of flower visitors to the flower traits of the plant community are not uniform.
We recommend that plant species to be sown in the field margins must be
previously selected based on their flower traits, to promote the presence of
specific flower visitors, which will ultimately sustain pollination services. In
this context, our study suggests that including crops with floral resources,
like legumes or mass flowing crops, like oilseed rape, within crop rotation
schemes, will be beneficial and promote a temporary increment on the
abundance of bees and other flower visitors.
200
Because agricultural intensification is also related to changes in the
composition of the plant communities located in the field margins, agri-
environmental measures must also be applied to mitigate it. However, a
different spatial level to the one of flower visitors needs to be considered. In
this study, we suggest that field management must be taken into account, by
incorporating low-intensity agricultural practices like organic farming, since
its effects on the plant community are the most intense.
Although landscape simplification under the current social and
economic conditions is difficult to reverse, its negative effect on fruit set can
be reduced by increasing flower resources availability at the margins.
According to our studies, the benefits yielded by this increment seem to have
far-reaching implications, as the effects on species of generalist pollination
are especially profound. Similarly, an increment in the proportion of
organically managed arable land at the landscape level only benefited
generalist plant species. Our study highlights how the incorporation of
legume crops provides abundant temporary floral resources that benefit fruit
set of entomophilous plants, in addition to agronomic services like nitrogen
fixation. It is important to emphasize that the observed increment in fruit
production is independent of plant pollination syndromes. Finally, by
incorporating mass flowering crops and maintaining floral resources at field
margins, it is possible to optimize pollination services through a broad
diverse groups of flower visitors in agricultural habitats in Mediterranean
landscapes.
201
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